Ecological importance of soil bacterivores for ecosystem functions Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart

To cite this version:

Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart. Ecological impor- tance of soil bacterivores for ecosystem functions. Plant and Soil, Springer Verlag, 2015, 398 (1-2), pp.1-24. ￿10.1007/s11104-015-2671-6￿. ￿hal-01214705￿

HAL Id: hal-01214705 https://hal.archives-ouvertes.fr/hal-01214705 Submitted on 12 Oct 2015

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Click heretoviewlinkedReferences Click heretodownloadManuscript:manuscrit.doc Manuscript Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 23 22 21 20 19 18 17 16 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1

4 Montpellier, France 3 Germany 2 Montpellier, France 1 Affiliations TrapJean Authors Ecological soil importance of Title 1 Number of appendix: Number of tables: 1 Number of figures:7 Number 157 (abstract): of words 8583 Number (main of text): words ELISOL environnement Dept. ofTerrestrial Ecology, Institut National deRechercheAgronomique Institut de Recherche le Développement pour Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

1 , Michael Bonkowski

Comment citer cedocument: , 10 avenue duMidi bacterivore Institut 2

, Claude Plassa

of Zoology of s on ,

ecosystem functions 30111 Congenies30111 – –

rd UMR Eco&Sols,Viala, PlaceUMR 2 34060, UMR Eco&Sols,Viala, PlaceUMR 2 34060, , University Cologne,D , of 3 , Cécile Villenave , France ,

4 , Eric Blanchart

- 50674 Köln, 1

1

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 45 44 43 42 41 40 39 38 37 36 35 34 33 32 31 30 29 28 27 26 25 24

stoichiometry Bacterivores Ke biomass effects ratios in C:N:P propose Bacterivores Conclusions effectsecosystem on functions. overview of the importance of U Scope their ecological inthe importance maintenance change biodiversity fertility involved insoil and plantproductivity B Background Abstract Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological acteri sing meta ywords

vores on and biodiversity soil erosion, it , a

and plant

new new soil Nand availability soil P

- analysis tools ; Protists, Nematodes; Protists, ,

in ; Meta mostly represented byand represented protists nematodes mostly soil soil theoretical theoretical soil soil contributed significantly contributed keysoil ecosystem functions. tonumerous ecological bacterivores , microbial responses in - analysis Comment citer cedocument: , w framework

factorsareexp that ea aimed quantitative synthesis at ofthe providing ecological

and plant

on

nutrition andgrowth.nutrition ;

ecosystem functions. We also We intended toproduceecosystem an functions. for plants Microbial loop; Plant growth Plant Microbial loop;

based on based

becomes urgent recognizeand suitably to quantify biomass , immobilization of Nand P , immobilization ected todriveof themagnitude ecological stoichiometry of ecosystemof

as important as

. I . ,

are a n the current context ofglobal context n thecurrent function parameters driving bacterivore ;

Plant nutrition ; Ecological ; nutrition Plant k ey component of soil ey ofsoil component s.

stress in

the bacterial ing bacterivore the role of the

We We

- 2

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protist evolution protist while flagellated, morphotypesandrepeatedly andamoeboid naked, testate origina soils ( traditionallygrouped ciliates, into flagellates, amoebaeandamoebae naked testate Bacterivorous are protists soil These bacterivores bacteri A threats coulddamageecosystemservices by accomplished the of understanding 2005 activity and distribution abundance, etc.) invasion, biological pollution, loss Unfortunately,soil services ( 2001 wide range of cansoil host global biodiversity S 1. Darbyshire 1994 Barrios 2007 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological oil key Introduction

s ; ( ;

( are some of ibeht 2012 Kibblewhite Geisen et al.2014 Wall etWall al.2010 component of vores ad e a. 2013 al. et Gardi ( de Vries et Vries al.2013 de

( 6000 different bacte Bardgett et al.Bardgett 1999 et ; protists Brussaard et al.2007

(

) the most biologicalthe most Adl et al.2005 . However, diversity molecularstudiesrevealenormous taxonomic an in s are mostlyrepresented by ofspeciesin terms

are

soil many roles of soil biodiversity is required in order to order in required is biodiversity soil of roles many , ) nematodes, enchytraeidsnematodes, . Through their activities, soil organisms. Throughsoil activities, ensurekey functions their soil

Comment citer cedocument: ; also also )

. biodiversity Geisen et al.2015 ay pressures Many ; among the most most the among ; ietl 2006 Pimentel Kibblewhite et al.2008 general ; rial genomes,rial ; Adl et al.2012 Bonkowski 2004

; have been been have ly

Waggal. 2014 et ly ly involved in soil fertilityinvolved insoil and plantproductivity (

( oso t l 2005 al. et Bossio

Coleman and 2015 Wall Coleman diverse unicellular unicellular ) si eoin ln ue hne overexploitation, change, use land erosion, (soil , and only areand theciliated , monophyletic, protists ; threaten protists

several metersfungala hundred of and hyphae environments, environments,

identified identified clgaesy t l 2014 al. et Schlaghamersky or mites or ) .

; heterotrophic Bonkowski et

ed and nematodes ) ) .

and contribute to manyandecosystem contribute to

environmen ( Jones et al.2009 Jones ; as soil soil uoe e a. 2002 al. et Dupouey

directly disturb directly encompassing of about 25% organisms. ;

Decaëns2010 eukaryotes, thatwereeukaryotes, al. 2009 ts ( Ronn et al.2012 Ronn

in terms of biodiversity of terms in

; ; Lavelle and Spain predict ing Brussaard 1997 ) ) A thorough A .

. soil organism soil

; One gramOne of Foley et al. al. et Foley ted during ted during how these these how are ) . ) 3 .

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 95 94 93 92 91 90 89 88 87 86 85 84 83 82 81 80 79 78 77 76 75 74 73 72 71

through computer investigatedWe the lit 2. Meta effectsecosystem on functions. the ecosystem functions using meta providing synthesis aecological quantitative importance ofthe of Bonkowski 2012 andClarholm Here, quantify ecological importance their intheecosystems. maintenance of expectedthat is toalter soil known yet,nematode specieshaveand described been their biologyecology and poorly remain ( Yeates 2007 nematode co individuals 2014 in terrestrial andsuccessful ecosystems colonizers of niches soil ( spe range)size form of andone monophyletic ahighlydiverse million group about including faunal biomass Despite ( their size small Coleman and2015 Wall Lambsheadet al.2004 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological cies ecological (biotic and abioticecologicaland (biotic ) . It than. of tensof estimated millions been has as a ( ( - Brussaard et al. 2007 Brussaardet al. Lambshead 1993 analysis analysis complement ; Yeates 2003 ( Bonkowski 2004 - searches

Data sources,Data analysis extraction and erature publishedin

) to Comment citer cedocument: . Both bacterial. - average size ; exist inonlyexist forest square one meter ) detailed reviews published inthe past ) Couteaux and DarbyshireCouteaux 1998 , makingonEarth onetaxa phylum oftheanimal diverse this most . Still, they. Still, remain toother soiltaxa poorly studiedincomparison i bacterivore n availableISI(Google of Web databasesand Scholar ) . It ofglobal. current urgent, change becomes context thus the in ;

- Bonkowski 2009 etal. analysis tools. We alsoanalysis We intended tools. to ) factors todrive oftheir the thatare expected magnitude ) . Nematodesmulticellular small eukaryotes are (0.03

2 -

- 50 µm), 50 µm), communities, tosuitablycommunities, recognizethespecies and to feeding peer - reviewed journals before Decemberreviewed before 2014 journals protists canprotists largely tototal soil contribute protists protists ;

Chen et al.2007 and nematodes arewidely distributed ) . Only a fraction ofand. Only aprotist

andof thousands hundreds of ( Cowling 1994 Cowling ( ( Bonkowski 2004 Bonkowski Cowling 1994 Cowling bacterivores produce an overviewof

) , we aimed, at ;

Foissner 1999 in ;

Geisen et al. soil on soil ; - 1 mm 1 mm ; 4

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response using 1 ratio Equation For directly orfiguresfrom tables, the 2.6.4 text PlotDigitizer software. using experimental information parameters, (soil species, protocols, etc.) recorded the and concentrations and shoot in root ratio)shoot:root and net Nmineralization, soil ( (measuredplate counting), soil by biomass (measuredfumigation or substrate by analyzedWe of effects the comparing low sieving measuring without thesoil thesuccess of seasonal soil cycles,oreliminated studies thatmonitored soil one function of and(iii) interest, reportedoftreatment meansc and manipulating soil effectsstudies that(i) tested the of alsoWe searched inthe studies reference ofrelevantWeselect lists and articles reviews. predators, earthworms, microbial nodules,nutrient, mycorrhiza, nitrogen, loop. phosphorus, biodiversity, bacteria induced thefollowing effects. used We key Knowledge),with norestriction microbial Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

each observation, we calculatedeach we effect observation, (ES the size individual

respiration divide respiration

mean mean versus bacterivores values ofthesevalues functions presence/absence in of plant plant ,

bacterivore high soil soil high Comment citer cedocument:

net P mineralization,net plantgrowthbiomass, P and root (shoot nutrition ( nutrition bacterivore bacterivores d by biomass microbial

in

bacterivore ( on the yearon the of Hedgeset al.1999 controlled , bacterial microbial bacterivores bacterivores

total expressed inmg

population changes orduringpopulation perturbation after

on 1 N and P

- - densities and modellingdensities studies. experimental conditions, experimental (alone soil, words or incombination): feeders 8 basal

- microbial and plant functions: soil microbial soil andplantmicrobial functions:

publication, thatinvestigatepublication, induced soilbacterial respiration), number

by adding biocides in the soil, freezingby inthesoil, adding biocides or on ecosystemsuccessfully functions by

the elimination.alsostudies We excluded

amounts respiration, /grazers )

. carbon

- N or mg or , protozoa, ), expressed inmg soil phosphatase activity, phosphatase soil soil - microbial metabolic quotient microbial metabolic P g P i ) from thenatural ofthe log - . 1 ontrol

bacterivores ). Foreach study,we These data we data These (ii) measuredat least protists, protists, . We excluded field excluded We .

bacterivore

- N or mg nematodes,

as well asas well re

extracted - P plant P - ed - 5 1

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lacking.Foreach weES calculated observation, the observations). include We didnot studiesw bacterivores andgrowth.plant nutrition collected We comparing studies from dataeffects the of alsoWe significance usingamonggroups matter with organic matterwith or databasegroups “agar” 4 according into (or tothe“sand” medium: “humus”, (m agarose), effect by ofthe mediumused the calcula Forzero. understanding a intuitive ofthe more effectsof ES (2) (999 iterations). the ba and negativePositive ES This metric “C” thecontrol (absence mean of (1) Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological cterivores

m equation the 2and estimated

was considered ( significant and/ ted the percentage ted the percentage ES ES determined the whether presenceofm i m

or = Ln= (T

reflects

= (Σ ES in ofon thefunction interest. thencalculated(ES We size the effect mean nutrient the rhizosphere infectednotby ofplants or mycorrhizal

i

a relative changeduea tothefunction presence relative ina of i / C ) / n ; with “n”) /n;with thetotalnumber ofobservation

solution). We thencalculated solution). i Comment citer cedocument: ) ; i

of changefrom control (%CC) indicated respectively andpositive a a negativeeffect of where “T” treatment was (presence the of mean nutrient P 95% experimenters the bacterivores

<

solution) andsolution) “soil” (aloneamended withsand, organic or 0.05) if 95%confidence its notoverlap0.05) did intervals with Kruskal confidence interva h ere control (non the - Wallis test Wallis ) for theobservationfor ) i. ycorrhizal fungi alteredbacterivore

in their studies. i

ES for mycorrhizal and m

l for each testedgroup for and from the ES bacterivores at around the P To doso,

<0.05 mycorrhizal mycorrhizal the the s

ES m

on functions, weon functions, .

level fungi (7studies, 14 We alsoWe testedthe m non bacterivores using bootstrapping we the split bacterivor .

- mycorrhizal plant) was - effects m es ) using . ) and also

ixed ixed on

6

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accomplished by these(witho organisms yearyears,a 1.1 papers period of per 37only using either herbaceousor (73%) woodyspecies. According (27%) toourliterature in survey, experimental co studies corresponding to investigatedeffects of bacteri collectedWe 4 3. Quantitativesoil synthesisbacterial of concentration wefindany ofdidnot Ninroots, effectexperi of which respiration ( was asymmetric, corresponding publication topossible bias,which was for each function of regression between the searched for p regression. biomass (explanatory variables). bacterivore induced effect ontotal N(or P) size Linear level. plants and tested for Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

ranged vores meta - The normalThe - induced effec induced P

regressions on ecosystemfunctions ( - ublication bias using funnel plots. We tested biasusing thesignificance We plots. ublication funnel ( from 3 to 561 days,from 561 3to value: 0.02) value: 1

experimental published studies ~93 ( Peters et al.2006 Peters significan % and and % bacterivores

- Comment citer cedocument: distribution inoculatedand bacteria we t sizes on shoot (or onshoot root)t sizes N(or P)concentration(root) shoot and bacterivore .

re to performed We alsoWe between testedthe relationships duration, experiment ~41 t

difference inES % of reported studies, respectively%1). Around ofreported(Figure studies, 6

95% intervals confidence for were calculated each and ES

on N and concentrations orplant P insoil (either on ) of residuals was testedusing Shapiro test.

amount . A significant regression thefunnel. Asignificant that plot indicated - Appendix induced ES ES induced ut taking into accountut takinginto books). We and reviews m

- values tested the relationshipstested between

bacterivore in shoot (or root) (responses variables)in shoot and the on

bacterivores m 1). Among 3 them, since average

using versus using regression. Exceptfor the 1977 investigating effects the ofsoil

the

literature focused theecological on functions the inverse sampleofthe size study Kruskal

in the rhizosphere ofplants, in the ment duration onES

8 -

Wallis testat Wallis and 1

the casethe for only 7

the P s tudies - Finally, we value

tissues . P

<0.05 6 % of - ), 7

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effectsecosystem on functions protocols species and the werenutrient highly solutions also different as among studiesasthe choice of well organisms amount (Tableand composition 1). The experimental devices dish (Petri instance, alsoWe food web experiments. conditions have certainlythe constituted mainobstacles inthe establ These methodological difficulties drawbacksstrictly withworking the under together sterile microscopy equipment toexpensive inaddition (high protozoology skillsand taxonomic andtime nematologyrequire thus specific nature at ofsoils the micro 1999 knowledge ismostly restrictedtofewcultivable species proti ( small in observing,characterizing enumerationand description) (extraction, manipulating and these This ecosystem functioning analysis significant criticallyregarding butremains rolesof organisms limited the these on believe studies(and thatthe number of observations) Cowling 1994 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

sts becausests themajorityfrom beextractedand oftaxacannot our soils, taxonomic ) apparent soil ofinterest in lack - . size

Furthermore, this practicalFurthermore, this difficultyand isenhancedopaque by theheterogeneous note

experimenters made d

organisms incomparison tolargersoilfauna ( d

that contrasting experimental protocols ;

duration duration the identification of ecological factors that are ofthe identification ecological factors likelytodrive Ekelund and 1994 Ronn Ekelund

(

Comment citer cedocument: Bonkowski 2004 used various types of medium (agar, sand, humus or soil) various(agar, typesor used humus ofmedium sand, of -

the experiment2to561days). (from spatial scale in contrast to aquatic environments. Soil toaquatic Soil spatial scaleenvironments. incontrast

more difficult es , g

bacterivores lass tubes,rhizobox ; ; Griffiths and Ritz 1988 Griffiths and Ritz Chen et al.2007 Chen et . On

can becan by explained the

the other hand, also it (C:N:P ratio) (C:N:P

- is large quality light have been ( es Ekelund and Ronn 1994 andRonn Ekelund e.g.

) or pots)growth for theof .

enough ameta to conduct arthropods or earthworms) or arthropods

T of organicamendments and ) used used . his high diversityhis high in - , This is particularlyThis is for true

or electron ishment of soil micro ofsoil ishment in these in these allowed us to usto allowed difficulties - bacterivore consuming studies. For - microscopy).

; or Foissner model

involved - - - 8

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in aparticular (orenvironment Kjelleberg 2005 capture mechanisms co differences in ( et al.1978 1980 bacterivore The effect of 17% ofcontrol, respectively 2). (Figure microbial biomass 1980 bacterialabundance reduction biomass) due (and cells toastrong of senescent However, a studiesshow number of Coleman et al.1977 induced microbial a or insoil reduction biomass bacterialabundance Because 4.1. Microbial biomass 4. conditions. estimate a Glücksman et al.2010 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological - Bacterivore evolution be ) ; , Ingham etal. 1985 incubation protists n ;

Elliott et al.1980 Elliott species ov bacterivores bacterivore erall erall - tween bacteria and protists had a major influence on the evolution ofprey major had influence bacteriatween a evolution and protists onthe effects on thesoilmicrobialeffects on communitynutrient and )

and feed presence nematodes onbacteria, the of .

time time In consequence, and bacterialabundance estimated by themeta bacterivore ( ;

Ingham etal. 1985 ( Darbyshireet al.1994 Parry 2004

; ( Comment citer cedocument: Elliott et al.1980 Elliott Griffiths et al.1999 ; -

effects on bacterialhasabundance been according showntovary to Sundin etal.Sundin 1990 )

or nitrogen - experimental effect representativeofarange ofenvironmental wide )

on bacterialCertainlyare abundance multifactorial. thelong and bacterialstrategies defense predicting

ed

that thepresence of ;

Postma ) ( , supply Baath et a Baath et ; ; ) Elliott et al.1979 Elliott set up) remainsset difficult. up)

. Ronn etRonn al.2002 bacterivore

The - Blaauw et al.2005 and availabilityand global l. 1981 - effect on soil bacterialeffect onsoil community effect of grazing on thesoil effect of bacterivores )

and ; ; Xiao et al. 2010 Xiao et al. ZwartDar and

these organisms usually organisms these - identity of ( analysis wasanalysis Jousset 2011 Jousset of labile carbonof ) , soil texture texture , soil (

Anderson et al.1978 Anderson

can lead tohigher can availability

bacterial byshire 1992 ( ) - Elliott et al. Elliott ; , 16% and 16%

Matz andMatz ( showing that Elliott et al. Elliott ( Anderson Anderson

taxa - -

; ) . 9

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chemical as the production such of protections, pigments cells toform micro such as different become grazing to means microbial in composition thepresence of grazingSelective has cells beenmainmechanism as causing of proposed the a in shift in presence ofnematodes composition amplification gene, of theamoA et al. Xiao ( function, such as nitrification bacterivores et al.2009 makeactinomycetes filaments suchas bacteriapositive proportio relative bacterial abundance dominant populations of grazing composi microbial effectson havepublished studies resolutioncoarse a taxonomic 2006 2013c of T 4.2. Microbial composition Djigalet al.2004 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological he whole ofthe composition microbial soil community in changed drastically protists ; ; Djigal etal. 2010 Ronn etRonn al.2002 bacterial shape and size size bacterial and shape ns ofbacteria aregrazingeither that by protected,gram physical suchas means,

; ( Bonkowski et al.Bonkowski 2011 et Jousset et al. Jousset 2010

to alter the composition ofthe microbial can biomass composition to alter feed onmicrobial back the of ammonia ( Griffiths etGriffiths al.1999 ; - Gould et al.1979 colonies, filaments or biofilms colonies, ; Comment citer cedocument: ; - Djigal Rosenberg et al.2009 oxidizing bacteria ( bacterivores

( ; Djigal etal. 2010 Jousset et al.20 Jousset et al. 2004 et ( Bjornlund2012 et al. ; - Ekelund et al. 2009 Ekelund etal. resistant, which canresistant,grouped which protections be inphysical

) tion ; . . (

For instance,For u Ronn etRonn al.2002 Rosenberg et al.2009 Rosenberg . Usually, thepresence of protists ; Postma ( 2010 AOB ) 08

; and bacterialand

Jousset et al.2006 Jousset ( ; ) Bonkowski etal. 2009 )

- ( et al.2009 Mazzola found inthe a significant shift

Blaauw etBlaauw al.2005 Bonkowski et al.Bonkowski 2009 et from

sing a basedsing technique DGGE onPCR ( limiting ourability assess accurately to ) Djigalet al.2004 ; , cell and wall resistance, theabilityof ; Griffiths et al. 199 Weekers et al.1993 Nitrosospira ( Weekers et al. 1993 etWeekers - ) feeding n , orby chemical means bacterivores )

or phosphatase activity

) sp. to ) . ematodes ematodes . )

Unfortunately, most , often increasing, the ) The ability of . Bacteriaevolved . ; 9 Jousset 2011 Jousset ; ) Nitrosomonas Koller et al.

and those that )

the or of specific changed the ( community Blanc et al.Blanc et presence ( Jousset Jousset ) - ; and

sp. 10

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bacterial strains nematode fluorescens populations of active continuously pumping pharynx Because like thick to consume bacteria with serves crushing for trappedbacteria addition, whi graspingand raptorial feeders ciliatesWhile trait involved inselectivegrazing aptitude interception,grasping, filter On the other hand, bacteria also 1981 ( resistant taxa bacterivores have been toxins Ekelund 1996 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological l gram e the digestibilityn and ;

ly diffusion and Blancal. 2006 et ( Jousset et al. Jousset -

select bacterivore bacterial certain - Caenorhabditis elegansCaenorhabditis bacteria. positive identified as

CHA0 in batch and CHA0 rhizosphere inbatch systems,

have been shown toconsumehave shown been

(

move out of toxic biofilms, move outof toxic Jousset et Jousset al. 2008 ; for for mildly toxic , confirming its Weekerset al.1993

b - acterivore specific prey feeding bacterivores

filter feedersfilter relyfree onthe interactions interactions 2006 ; main driver main Comment citer cedocument: VenetteFerris and 1998

; utritional values an ofpreysconstitute important trait involved in nematodes nematodes Jousset et al.2009 Jousset

wild -

nematode , diffusion rather

cell walls t

lack in taxa taxa ( have forms different developed offeeding (direct - Ferris et al. ( ) typeand non Pussard et al.1994 .

did not vary with changes varydid not with inthefrequency the two of The ingrowth differences of rates s

)

( such as protists of changesbacterialcommuniof in

rely on bacteria they can dislocate from biofilm surfaces biofilm they onbacteria canrely from dislocate Fürst von LievenFürst 2003 von and nematode can

- taxa selective

or raptorial feeding);or appears this ingest ingest hat are for largelyundigestible bacterivores, other amoebae ( preferentially

Parry 2004 Parry evolvedgrinder awhich inthebulb terminal ( 1997 ; - toxic gacS toxic Mazzola et al. 2009 compared to around around - ) swimming bacteriaswimming

according tobacterialsuggest species that ) , i

graze and biofilms within directly . populations ) Jousset etal. t appear . showed that

; Ronn etRonn al.2012 20 cells the competitors of thegrazingthe competitors of - deficient mutants of deficient mutants ) , thus providinga means, thus physical s Acanthamoeba castellanii Acanthamoeba

unlikely that nematodes unlikely that

( during Anderson andAnderson Coleman

the diet composition ofthe diet the composition ( ) 2009 .

In particular ( ty composition, sincety composition, bacterivorous bacterivorous Ronn et al.2012 Ronn each suction each ) ; , using mixed mixed , using

Weisse 2002 as an important Pseudomonas ,

the latter protist of their

) ) - . .

that In

11 ,

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nutrient The effects of bacterial undigestedfood labilecarbonparticles, with higher activity metabolic bacteriv bacterivores indicating relative to respiration analysis that revealed t ( T 4.3 Microbial activity bacterialcom rhizodeposits Lastly, thereby developmentprobolae of cephalic support high variations are likely more to clearly non preferred the Alphei etal. 1996 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological he presence of bacterivores s ores optimizing niche partitioning niche optimizing among availability

this hypothesis.this He re

that the microbial carbonthat themicrobial microbial biomass - and growth

canyounger senescent ingest and tomaintain contribute bacteria bacteriacells ( munity Manzoni et al. 2012 et Manzoni ( bacterivores Sundin et Sundin al. 1990

microbial turnover,microbial measured as in theshape head species ofCephalobidae bacterivores alter b ; ( Coleman et al.1978 Coleman ( have beenhave suggested to Griffiths 1994a Griffiths Clarholm Clarholm (

Benizri etBenizri al.2002 and nutrient and nutrient he presencehe of Comment citer cedocument: - acterial toxic bacterialtoxic mutants.

on microbial communit investigated indetail

generally carbon (see 1985a community ) ; , which inturn can at the Sinsabaughal. 2013 et availability discussion in discussion - ;

use ef use ) Pussard et al.1994 ;

bacterivores by Koller 2013b et al.

enhanced overall activity the microbial and nutrie

; ; nematode headspecialization, food allow passivenematode +29% Djigal et al.2004 Puglisi et al.2013 ficiency (CUE) modify the amount andmodify composition the composition composition co

- and 35% and microbial metabolic quotient microbial occurring bacterivore

Bonkowski (2004 Bonkowski Accordingly, b nts makingmore favorable themedium for

how the probolae shape labial and of the t significantly inc ies feed back

have strong consequences ) . of ;

) throughmechanisms passive strongly recorded . Kuikman and Vanveen 1989 ;

The main mechanisms areThe that(i) mainmechanisms control ) Kuikman et al. 1990 Kuikman et al. .

on acterial the composition ofthe composition the ) reased soil soil reased , respectively decrease ) by De Leyby De

and (ii) theyandrelease

nematode species.nematode - feeding nematodes s

in presence of ( microbial respired ( and turnover 1992

) for for (Figure 2), (Figure of . T he meta soil soil )

. -

; carbon carbon The basal Xiao

- he 12

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prey Telegdy presence of microbial ( Furthermore, t N r 49% and 9 Ferris et al. Liptzinand 2007 global microbial soil stoichiometry steinii found Darbyshireet al.1994 part of stoichiometric homeostasisrelative totheir food 86% efficiency Using stable isotopes oftheand microbial stimulation activity according to effects mineralization et al.2010 Coleman et al.1978 atio Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological excreted by . However, s )

for

of mass C:N mass C:N

( the on soil nutrienton soil ciliate) and ‐ both Kovats 1932 eight

C:N ratioC:N ) of - ingested N . 20% of assimilated 20% of ( bacterivores

We found that the foundWe that 1997 the consumer the 37

bacteria he

the ( bacterivo % x 1.8 x the ratios of ratios of ; p ) . bacterivores Xu et al.2013 , we , resence of Ferris Ferris Rhabditis Rhabditis . In ratio the C:N ofbacteria. addition, ratesrespiration determines in the soil microbial soil ; , Crotty et, Crotty al. in absence ofplants) ) ; will bewill ultimately Levrat etal. 1992 and and

availability leadingN release by ratios C:N tohigher ofthe bacterivores at narrow calculated Ferris etal. 1997 Comment citer cedocument: , with C , re ( 3.5:1 - 1997 bacterivores nematodes driven nutrient recyclingdriven nutrient bacterivores sp. (

- , ( presence of ) N Elser andElser Urabe 1999 4.7

- ) found losses

bacteri for amoebae,for c and that biomass C:N:P

do exist simultaneously:do exist (direct excretion of nutrients way) (

:1 a (mass ratio C:N 2013

production efficiencproduction species. species. theoretical

nd

higher will will increasing )

; released by vore , and turnover )

Ferris et al.1998 Ferris leading to lower leading 5.6

found will (Figure bacterivores thus

:1 for nematode), respectively.nematode),

production efficienc production increase and respiration turnover microbial Because , iliates andrespectively. nematodes,iliates that soil protists protists soil that

directly of amount influence the

and and ra has been showntobe at decreasing ratios C:N 2). Two main pathways of Naegleria gruberi s nges bacterivores

( rangingfrom to7.4:1) 5.5:1 CNR

loose ) as .

bacterivores almost doubled almost doubled

quote of N excretion of ies ) ; microbial CUE andmicrobial CUE

carbon torespiration, due theory theory Griffiths 1994b from Crotty et al. from Crotty d

earlier

( only Anderson et al.1983 Anderson ies ( Elser and Urabe and Elser 1999

have have

( ( have have

ranging from 58% to fromranging 58% amoeba), Using recent values ofUsing recent values (indirect way). would be would relatively soil N(Nsoil to maintain to ( ) a production De . Borkott bacterivore

a decreased ( 2013 Colpoda min

assimilated ( 23 stable Cleveland )

- T 32%, 43 ) a great (

he

1989 ; and -

C:N C:N )

) 13

- -

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 343 342 341 340 339 338 337 336 335 334 333 332 331 330 329 328 327 326 325 324 323 322 321 320 319

resource availability ( explaining whyAnderson efficiency (NUE) proportion oftotalN) a Panagrelus redivivus Ng µmoles 1983 considerableorganicamounts ofN rangingand 0.0058µg 0.0012 between Ferris et al. importanton the consequences in rich ribosomes. decrease Indeed, rategrowth hypothesis of inline the requirements) (copiotrophs microbial community structure However, then elements excess in their stoichiometry, m strict homeostasis compared res toits mmonium mmonium Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

presence of be ) . Wright come with increasing

small changesofmicrobial biomass stoichiometrycanafter sh occur - ( contributed 23 1 ) havesuggested been

1998

available for nematode fresh

than slow than bacterivores ( 1975 Therefore, inthe dominance shifts of ) in order in order in respect nutrient to availabilityin soils

ource calculated that depending on their CUE )

i.e. were composed of found that found icrobes can regulate their by nematodesby may Comment citer cedocument: -

growing on ( growth rates synth demands toelevated the due for Pfor when bec nematode populations

ClevelandLiptzin and2007 et al. to balance their roots -

35% can wt

content transfer to ( ( in presence of Faninal. 2013 et of totalN 1983 hour that bacterial

to exhibit low exhibit to (Norg)

es (oligotrophs) es (oligotrophs) 3 - ) 1 -

)

- obser 14%, of N and P of N and P N liberated urea, occur when nematodes exhibit high whennematodesoccur exhibit - shifts in microbial biomass in shifts ind. stoichiometr - release canreleased be

feeding nematodes

( ved declinesinexcret (GRH) Mooshammer etMooshammer al.2014a 15

- amino acids amino bacterivores 1

- nitrogen day 34 er ratios (higher biomass C:N:P nutrient ) in Ringer solution . . For instance,

available fo % and 35 Large releas

- ( 1 (

Elser etElser al.2003

Elser et al.Elser 2003 et fast ; accordi

y Xu et al.2013 - to use efficiencies - a

me ol

or slow or by

and protein ( bacterial biomass ( Griffiths2012 et al. Kuzyakov and Xu 2013 and Kuzyakov - ng tospecies 45 nematodes

r plant growth r plant excreted N excreted e % of the total N the total % of

der). s fast

of - ion growing bacteria induced by the nematodeby the - organic Norganic ) growing )

Knowing that ; stoichiometry,with ; and ; and of Norg , N:P ratios , N:P s ) Hodgeet al.2000 , respectively .

by The e The ( , but , H Anderson et al. microbes 4 relea - .

C:N:P

N nitrogen bacteria with xcess ifts in the ifts in in addition, in addition, (in to

) with rate (mean 13.7 . s

esis ofP To ing in organism decreasing

dissolved dissolved ) ratio , while tal and in N .

maintain keep

-

use may s ) s .

, - 14

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nematodes, respectively excretion 2007 Applying therefore species Ncycling.soil Foral. instance, Ferris et c experimental (Figure 4.A). highes alsoWe bacterial N contrast, in bewill bacterialgrowth (mean ~ 3.A). was whil very tohumus, incomparison high interval Interestingly ge effects up Norg lassification of Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological nerally by ;

H (especially lowmolecular Ncompounds) weight plants Crottyet al t values were found whenwere found both t values

on soil Navailabilityon soil mostly N by limited umus umus . to

15:1

found thatp In parallel

remains difficult, especially difficult, aremains when mixture of focus would be the same net Nmineralization immobilization immobilization substrate , we found a greatwea found variability, inES ) (

had Gallet parameter themagnitude explaining of Accordingly, t and sand exhibited intermediate exhibited (mean values and sand ~20:1). ed bacterivore in . 2013

the highest the highest on , stoichiometric stoichiometric subs

- 27 we found thatw found we

Budyneket al. ly on ly rotists exhibitedsignificantrotists effects onN higher thannematodes with with - 48%, 73 48%, Comment citer cedocument: ; trates . Ferris et al.1997 These estimat

low C: NH should decreaseshould , leading to s is s is he choicehe in likely have likely have mass with high C:N 4 . Predicting . -

byfar 81% and N reasoning C:N ratioC:N

ratios 2009

hen the bacterivore not accurate not es are rapid immobilization of rapid immobilization be ; ( bacterivore 1998 (soil) 66 Nasholm etal. 2009 Nasholm ; en bacterivore Xu et al. 2013 Xu et al.

( - s substrate e exhibited intermediate insandit values (Figure as

ratios ratios Ferris et al.1998 Ferris 7

higher than for N (except for nematodes) thanN (except forhigher for under ( 6% ofassimilated 6% ) mean , bacterialgrowth

for N for i found highfound variation

for N

groups themicrocosms present in were enough (humus), -

estimated because species appears as anspecies appears asimportant ~39:1) while soi bacterivore

( used min Borkott 1989 Borkott - canre be effects

bacterivore as shownby95% confidence the ) , theoretical to in and in absence of livingand inabsence roots, predict experiment

) ; on nutrient availability .

Neff et al. 2003 Neffet al. N released - - - used by soil bacteria by soil orused P forP amoebae effects will be will ;

We We

species is used. is species ClevelandLiptzin and how of different l s had s had ranges ofexcess ranges experimenters

on N on therefore suggest limited bylimited s

bacterivores

was soil, by the lowest ones min bacterivores ) , ciliates and , . ,

nematodes nematodes The bacterivore

C the ES min

broad and

impact while - but the P taken taken

that . In. m

15 - ,

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95% confidence huge notexhibit did interval though variation ha factors many ecological withoutaffectingbiomass (+21%control) of theshoo meta 2001b ( P androot growth 5.1. Plant architecture 5. overall positive 2011 solution inthesoil mobile and can rapidly adsorbed be of ratio environment,C:P b ratio islow) the differentiating (adsorption (microbial immobilization The theoretical analysis? excretion rates of control) N(Figure incomparison 2). to in the meta Alphei etal. 1996 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ositive effectositive of Bacterivore excreted C: - ) analysis revealed a significantanalysiseffect a revealed of , reinforcing P ;

Irshad et al.2011 ratio ishigh

-

P fromP analysis of P

we found

gross - liberations effects net , leaching bacterivores bacterivores

; rapid bacterivores effect of effect , ), Djigal et al.2004

from from we foundwe the the

a on plant performance plant on Comment citer cedocument: positive effectpositive of immobili acterialgrowth ; bacterivore

Jentschke etJentschke al.1995 , microbial C of N of net of N and by P bacterivores

effects of on plant growthon plant ha

, etc.) afternutrient excretion occurring by not match with not matchwith l

ower may zation

- have ; bacterivore effect onP Krome et al. 2009a Kromeal. et UE, resource stoichiometry, etc.

Why

bacterivores may b of

bacterivores on P bacterivores occurred. occurred. P

did in the microbial and biomass bacterivores min

e N )

mostly limited byanmostly P limited min plant species details). (see1for Table the min - . ve

effects

and P se

was negative

been obse However on nutrient availability

t:root ratio (Figure 2). Interestingly, ratiot:root (Figure 2). the

biotic takedid not account into th on P by

eoretical on min

) on shoot (+27% control)on shoot root and of soil colloids soil

and woody min

P data provided by themeta

, i

mineralization rved (Figure Hence, inahigh 3.B). n contrast to N,Pis n contrast to ,

difference while i for both herbaceousfor both d rapid immobilization immobilization d rapid ( ( ) and abiotic processes) and Bonkowski etBonkowski al. Hinsingeret al. n bacterivores

hampering soil (wheresoil the . s

I (P in n

min humus (where (where humus N and N )

(22% of poorly

the

, - P Our thus ve C:

16 P

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the totalvariance ofES conducting linear highly variable and not increase amount ( plant nutrient when acquisition protozoaand nematodes The nutrition 5.2. Plant ro presence ofmycorrhizalfungi reduced usually the factoronlynematodes of increased 2.5, et al.2011 nematodes but among studies(Table number of rooteffect by ofcontrol. tips positive 96% However, this Kreuzeral. et2006 profoundly Besides biomass, biomass ( shoot effects and nematodes root induced been Bonkowski et al.Bonkowski 2009 et Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ot length,

positive effectpositive suggested were

of N androots, inshoots of plant inshoot Nconcentration ) . For instance, while . For root architecture byrootproduction promoting lateral

root significantly significantly to

Figure 4.B; in area number and a lesser extent than a extent lesser the presence of meta the literature toaffect s )

of (Table (Table 1 - bacterivores

) ). Shifts in root in archShifts ). m Comment citer cedocument: regressions, we found that ~34% ( foundregressions, that we fr different .

on total N Generally, w larger P 1

growth ). - value =value 0.109). Based on protists protists (Figure 4. (Figure i.e.

protists of root tips om 0(no

on plant biomass on plantbiomass

amount

of similar magnitude, +59% o +28% and for e found substant the number oftips the increase

bacterivore 11 protists

in the rhizos s C

bybacterivores

itecture werealsofor observed bacterial

n ). We did not findsuch). We didnot studies in shoot (response byin shoot explained was variable) - .

significant effectsignificant onth

d (

Chengal. 2011 et the number the bacterivore , we found that - effects could phere ofplants showntoalter hasbeen ial f control (Figure 2) were bacterivore P but when both by a facto

was large was <0.001) and ( <0.001) ~65% be on plant growth. on plant

inoculated in the soil thesoil inoculated in of most length,effect onroot specific root ( bacterivores Jentschke etJentschke al.1995

; ly a i n wa r of 1.2 (Tabler of 1.2 Irshad et al.2012 s variable) - (+25% ofcontrol) tips tips

effects related to related additive effect s greatly variable were on average . Although

Both, p on thetotal

present, their increased the . B . P increased <0.001) of <0.001) of y - 1 feeding rotists

). The ). The by a for

; the Irshad ; it was

17

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differentfrom 0, effects of related carbon toenhancedrather plant nitrogenfixation uptake than and Koller et al. rate wastissues internal plant cycling by Inrespect to weregenerally theeffe than larger nematodes mightwhy and orprotists, combined explain bacterivoreg effects the ofboth architecture nematodes were inoculated. Namountshoot was mostly caused byconcentration higher N nematodes Interestingly, increasedof N. concentrations ornematodesprotists neither was paralleled increased by an totalplantN,nor uptake by of (1991 variance inES increase total 5 respectively bacterivore Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological .A) 38% andcontrol 55%38% of s . These results. These shoot via photosynthesis) while themore gain was allocatedvia photosynthesis)ofP ) andet where production al.(1996) increasedbiomass inpresence Alphei plant of d

bacterivores the

N - than with , the data suggest, thedata mostly , effect onshoot

P, wethat P, found without significantwithout interaction thetwoexplanatory variables between a shoot we found m mount

for Nconcentration shoot ( suggestin 2013c

allocated imply N amount byN amount increasing shoot

protists (Figureprotists 4.C) by increasing of

on shoot P concentration P on shoot variable (+30% ofcontrol) less were ) Comment citer cedocument: higher shoot N concentrathigher shootN

newly showed thattheef

that in some experimentalthat insome g that biomass andshootNconcentration (explanatoryvariables), , respectively Togetherwi to

different mechanisms ofplant responses mechanisms different tobacterivore bacterivores

- shoot acquired N a acquired N surplus cts of either group alonects ofeither the

s

(probably the carbon maintenancefor ofhigh fixation shoot N concentration while in others, concentration whileinothers, N shoot th the lower effects of P (Figure 2). (Figure . These results . These .

made increased the increased Exceptions areExceptions et thestudiesal. byKuikman fects of protozoafects onplantperformance of more were nd P: nd P: available ion the biomass

conditions The data suggest s bacterivore

in experiments with in experimentswith

total suggest by , explaining whywe found high .

bacterivores amount s in plant tissue s inplant , nematodes onrootnematodes ed bacterivores to - induced induced

that the increase in total that theincreaseintotal roots. .

Compared Compared of P in shoots and shoots rootsof Pin differen

Krome et al.

was gain ofN inplant ba

enhanced the cterial

bacterivores ces inthe when

commonly to N,the

(Figure - feeding

and ( 2009a r oups

18 )

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6. Relati effects oninteractionsplant fitness on and herbivores with and plantpathogens. effectsplant reproduction on in contents tissues in in plant fitnessmuchmore might increases beprofound than ofplant and/or biomass nutrient treatmentsandgrown sterile bacteriarespectively with plants, production of 2001a barley plants andearsincreasedweight theindividual seed thenumber(+60%), seeds of (24%) (+32%) leadplants will to effectsIt biomass of and surprisingonnutrient not thatpositive uptake is ofbacterivores reproduction5.3. Plant &defense bacterivore concentration inplant tissues (without conditions interaction twoexplanatory between these variables biomass androotconcentration P (explanatory significant respectively variables), without total P regression increase concentration effect in root P (+23% this control), of was concentrated inplanttissues Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ) . More recently, et. MoreKrome al. amount onships between onships

, which tobe remain s - howed effects , and the crop wascrop , and eventoaphidherbivores thetolerant more Arabidopsis thaliana Arabidopsis

in root increase

that ~16% ( that ~16% on plant biomass (and biomass on plant dicate. s

(response variable) by explained was Comment citer cedocument: d bacterivores

U . plant repro .

A nfortunately, twopapers these only More studiesare certainly needed toinvestigate bacterivore P lthough known <0.001) and ~75% ( and<0.001) ~75%

(Brass

( 2009a , affecting

duction. For instance, For protozoa thepresenceduction. of the presence of may thus

and and increase icaceae) )

showed that showed root

plant biomass)and plant

favor favor -

infecting symbionts infecting total Nand P more than3

(Figure 5 P <0.001) of the total variance the<0.001) ofES total of bacterivore bacterivores A. castellanii bacterivore .B) . - These results imply results gainsThese that

and 7 amount .

investigated investigated Some - highly variable effects

other led to -

fold comparedfold to

( enhanced theseed Bonkowski etal.Bonkowski

- experimental in plant s effect

an important may on nutrient bacterivore

s promo

s

on root ). .

The meta The t e

m s

of on 19 -

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fungi. through more rootarchitectureon plantnutrition complex b thus can the stimulating effect of architecture populations. Second partner amount ofcarbon fungal symbionts the by estimated of bacteria and of mycorrhizal fungi is bacterivores Wallenda and Read 1999 enhance plantNand acqu P al. 2006 away by plantroots,and from releasing carboxylates nutrientlow soil availability consideredThe rootsis formation as widespread of mycorrhizal themost ofresponse plantsto 2008 plants are shortcoming natural in more knowing conditions, that, than rhizosphere of The effects of 6.1. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Bacterivores )

and ( ; Meier et al.2013 Meier Louche et al.2010 that ca. 7 infected by ectomycorrhizal

( on plantperformance through twomainpathways Brownet al bacterivores non bacterivores

& fungi Mycorrhizal released byreleased e root - - mycorrhizal plants (84%mycorrhizal ofreported studies) (Figure 1). 30% of net carbon fixation 30% ly soil fungi soil , mycorrhizal fungi, mycorrhizal a priori Comment citer cedocument: bacterivores host plant host . 2013 . ) ; . The presenceofmycorrhizalfungi altereffectspositive can the of

Olsson etal. 1996 on plantfunctions been have mostly investigate symbioses

isition isition ) clearly depend on plant carbonclearly depend onplant , mycorrhizal fungi ( Plassard et al.Plassard et2011 )

, mostly likely po toreduce the . Usually, presence mycorrhizal the ofthe symbio ( ( Plassard and Dell 2010

xudation xudation Jones et al.2009 Jones

on lateral root production (Tableon lateral root

( Marmeisse et al.2004 Marmeisse

form are known to are known ) ing will will

wit will bedirectly

have beenhave shownto often arbuscular mycorrhizal ) h indirect detrimental effectson decreas . Byvolume ofsoil a prospecting large ; ( Leakeal. 2004 et sitive effectsitive of Finlay 2008 profoundly rootbiomass and change e

; in

allocation toroots allocation 80% of herbaceous and80% woody of herbaceous Tibbett and Sanders 2002 ) the . : a

allocated tothe

t presence ) a

and enzymes first glance, thepresence e altered by mycorrhiz bacterivores 1 ) ). .

( Itis Smith andReadSmith Bacterivore of significantly d

This is aThis is severe in the a likely that . It hasbeen mycorrhizal root ( . The growth. The nt bacterivore Courty et - infecting reduced ;

effects the al 20

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nutrients can be re the acquisition of some organic N etal.Sundin 1990 organicare acids) N (amino by released Plassard et al.2000 presence ofmycorrhizalfungi It well knownthat is t interaction withbacterivores studies are phylogenetically constitute andthis physiologicallydistinct, mycorrhiza) on was todistinguish possible not mycorrhizal theeffectofeach simultaneous exploitation relationships. ofboth mutualistic bacterivore formulated etal. by Bonkowski fungi plants infec nutrition the positiveeffect of but substantialfor rootbiomass ( 6 were significantly or find any However, this Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ). This total amount ( Bonkowski et al.Bonkowski 2001b et negative negative were

required, especially ted by arbuscular mutualisms complementmutualisms each plantresources and are other allocatedtooptimize

a still still

in plant tissues. bacterivore priori

effect ofmycorrhizal fungi onES effect of mycorrhizaleffect fungi of on ; - reduced maintained used ; Wright 1975 Wallenda and Read 1999 bacterivores he abilityhe ofplants take to

hypothesis could not beconfirmed by Comment citer cedocument: by

when association fungi withmycorrhizal theplants were in (Figure - rhizosphere effect sizes. Knowingthat effect sizes. .

( . The Koller etKoller al.2013b ; ( those focusing on those Cappellazzo et al.2008 Cappellazzo Irshad et al.2012 Incontrast, ) ( - , we 2001b

- 1 on root growth, theeffects positive on root of

04%) (and P maybe

few existing studies support this hypothesis supportthis existing studies few expect

) bacteria

, showing bacterial assuming that the assuming the ES

that thepres ) . Because significant amounts of dissolved . Becauseofdissolved amounts significant . up up bacterivore ; Mycorrhizal p - -

) different myc types of ) forms) released by feeding nematodes . Koller et al.2013c m that even m These the hypothesis results also support organicN isgreater N as sourceof in

of

was very( biomass lowfor shoot both fungal symbionts ; bac Nasholm etal. 2009 ence ofmycorrhizalfungi terivores mycorrhizalthe and

Because

s when effect

the meta a serious shortcoming fungi(arbuscular type lants could thus s mycorrhizal fungi mycorrhizal

on N and P concentration P on Nand on shoot androot biomass on shoot

studies ) ( bacterivores

- Anderson etAnderson al.1983 and analysis. o bacterivores r r

ectomycorrhizal hi

; are lacking, it zal fungizal Neffal. 2003 et are

bacteria gain We did not didnot We for both , before . M will will - a

, reduced on plant or or in - 5%) ore - favor ecto ; 21 - s ;

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 543 542 541 540 539 538 537 536 535 534 533 532 531 530 529 528 527 526 525 524 523 522 521 520 519

7.1. 7. proxy how topredict efficiency areformed. thenodules once The availability P soil average al. 2002 of energy take transfer placenodule inthe symbiotic symbiotic efficiency Nfixation usuallyrequires high can notjudge theside root nod rhizosphere of Alexander bacteri functions ofterrestrial ecosystems. hasgiven been attention Yet, little Because plantproductivity, Nusuallyone is limits ofthe important biological Nfixation most 6.2. improve notbeoverlookedshould find experimental study hypothesis this testing competitive advantage microorganismsf over Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological A ‘stoichiometric S Bacterivores toichiometr vor ) by 22% of control. by 22% of ules and . mycorrhizal plant N mycorrhizal plant

The meta es ( 1980

on symbiotic N fixation and legume Nfixation on symbiotic growth ( Phaseolus vulgaris Phaseolus )

ic control growthof

& N and subsequent plant P acquisition and plant P subsequent showed that showed - analysis showed that bacterial analysis showed thatbacterial ’ bacterivores - 2 perspective on effectsno protist ofthebiocide, since - fixing plants fixing Comment citer cedocument: ,

andwhich maymechanism an constitute by important s

P. canWe hypothesizethat on

nutrition. vulgaris protists protists bacterivore

. Lennox. and in the vicinity of nodulesin the vicinity may of

bacteria

decreased whenused they - effects N:P ratio ofnodules would ratio N:P or soil Nreleasedor soil by , -

Alexander Alexander but we believe N organic circuit thatthis bact

the abundanceroot of

on s bacterivores erivore , protists protists ( levels might Drevon and Hartwig 1997 Drevonand Hartwig oil oil a biocide to suppress biocide tosuppress Appendix 1 Appendix nutrient availability ( 1981 of - - pr and nematodes, by increasing plant interactions plant specific exist biocides omote higher N fixation Nomote fixation higher available

increased soil P availability P increased soil ) affect

found higher found higher bacterivores ). to - plant N plant

Ramirez and nodule bacteria inthenodule P then then the potential role of b ecauserates high protists be an important

uptake . We did not didnot . We numbers of

; bacterivores Vitousek . H , butwe . igh

et on 22

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Clarholm 2012 by during plantroots,or derived mineralization bacterial N C:N with low of rapidnewly immobilization (4) al. 2013) microbial stoichiometrycan after occur themicrobial shifts in structure community (Fanin et al. 2003 (3) theavailablehomeostasis with N elements in ( Microbes ( P comparisonrecycling in to soil bacterivorenematodes. microbially to immobilized ratios. C:N:P Th bacterivores release lowbeen production showntoexhibit efficiency (1) of stoichiometry Comparing of thedata bacterivoreeffectsN on ClevelandLiptzin and2007 2 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ) e

S Bacterivores Bacterivores Bacterivores

amount oil s withhi ) ,

caused by bacterivores are C:

and P s ofN excess depending ontheir CUE N:P ratios organismN:P in

For example, et Cole al. strongly or C:P

) thereforedepend intermsC, onenergyoflabileplant available .

gh or C:N C:P

have to maintain to have can alter the soil microbial thesoil alter can community structure. often if we to want if

immobilization -

and P a

ratios

great part ofingested N increas homeostat Comment citer cedocument: - release are may induce )

e and can -

predict ratios mineralized N mineralized microbial . ic

initial - .

st T and P

in terms of their biomass C:N:P vary oichiometric homeostasis

he net expected to may

( how regulate their regulate their

1978 phases decomposition oflitter energetic starvationenergetic for - with growth rates.with Therefore, levels in soil (Griffiths soil in etal.levels 2012) turnover

be effectsof

bacterivo

) (

Mooshammer etMooshammer al.2014a nutrient nutrient

showed thatamoebaeshowed were efficient highly at or P or and P P and -

and P and ( vary Crotty et al.2013

and from nutrient in mineral form res bacterivore deficien

-

according to further availability important toan point

impact functions ecosystem bacterivores - use , butespecially haveprotists t decrease decrease

for bacterial growth bacterial s

efficiency on soil N and P N on soil

According toGRH bacterial growth bacterial

) bacteria andbacteria at the community scale .

( ( According

Elser andElser Urabe 1999

Ferris etal.Ferris 1998 ( s Bonkowski andBonkowski ) microbial microbial mall changesmall

leading toastrict by .

releas either provided , reducing ly bacterivores CUE.

, . favoring ing

in ( Elser etElser )

. S role

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above ( growth null is which plant From graph, this definedthe“critical we (R ratio” presented by increasinggrowth rate plantrelative Zechmeister elements Ecological believe partitioni byexplained Nconcentration higher shoot we showed N thattheincreaseintotal same magnitude to plants and areexclusive ofeachHowever, not itis other. andnutritional non st where Bonkowski n andgrowth.nutrition Because described quoted earlier, mechanisms, nutritional by which bacterivore Clarholm 7. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological utrient concentration rong consequences 2 . S toichiometr protists increase rootbranchingby protists lateral d

that ng inexplanatoryvariables for the growth of growthfor the (

1985b s stoichiometry describes between ofthestoichiometry relative theimportance proportions (

- 2004 impact plant Boltenstern et al.2015 Boltenstern Ågren ecological ) ic controls )

and Bonkowski

- proposed a hypothesis ‘hormonal’ proposed bact

nutritional mechanismsnutritional ( 2008 on s

( erivore Comment citer cedocument:

stoichiometry plant internal metabolism auxin Alphei etal. 1996 functions )

organisms as

on a - bacterivores bacterivore effects linear relation linear nutrient ( . 2004 )

T . ( for for Agren 2004 P he ‘soil microbial loop’hypothesishe ‘soilmicrobial (

can helpcan amount under different Elser et al. 2000 etElser al. lant C:nutrientratios bacterivore )

proposed theoretical describproposed frameworks ; limitation)

- or can enhance root growth enhancecan increasing without root Jentschke etJentschke al.1995 effects will will ship higher shootbiomass.

in shoot to occur concurrently of inthe rhizosphere alter ; cri

understand between these two plant traitsbetween (F twoplant these Elser et al.2000 on p - ) which designates the effects ing .

based onnon experimental conditions. s ; lant lant

induced Gusewell 2004 ( microbe unlikely Krome et al.2009b

bacterivores n on areassume utrition andgrowthutrition th total ese ; by - Kuikman et al.1991 Kuikman root communication that they contribute that they )

-

pattern . This was conceptually. This P nutritional mechanismsnutritional bacterivores We foundWe s amount in roots in amount ; d

may plant increase

Sardansal. 2012 et

( to Clarholm 1985a Clarholm s C:nutrient . decrease with

) . B For instance, imilar imilar

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) to , how

We We , with plant the 7 .A). .A). )

; 24

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synthesis. investment T and relatively C more T to two parallel processes,an presence of release inmicrobial befixed biomass duetonutrient ofroot could C not Subsequently more recentl of bacteriaand theamoeba quality,LQ) low ratio C:N (hig or plant are available plants, poorly for Under t more conditions naturalsoil uptake fromdepleted the amendments is of nutrient addedhigh supporting tosoil, levels of biomass. bacterivore assumed tobe Forcertain a t plant species, Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological he formationbranching andthe resulting oflateralroot requires roots he non wards rhizosphere C the s is s is plants, , and - strong nutritional S Manipulating nutrient availability throughManipulatingaddition ofHQ to soil, litter to plants the s uch conditions are

of photo activity bacterivores causedbacterivores by bacterivores nutrient release will be will nutrient furtherinpresenceenhanced release of y , they fixed 13 nutrient availability insoil .

For example,For CO

showed that plants in presence thatplantsin showed of high substrates allocated ratio C:N 12%

2 rely on arely synthates mechanisms suggestmechanisms photosynthates toroots

respiration losses from more the soil thandoubled, - - fixation fixation allocation. Comment citer cedocument: A. castellanii increased nitrogen and uptake

he ( Bonkowski etBonkowski al.2000 relatively experimentally and nutrients: Koller et al.

before major cause natural planttissue highin of C:nutrientratios i.e. a ,

17% 17% inoculated soil withbacteriawith to h quality, HQ) or

microbial biomass turnovermicrobial biomass when competition for Nand between P

he nutritional mechanisms or without or ,

decrease and high release ofnutrient release high microbial microbial

that (

( Ågren 2008

2013a planted with in presence of protists in presence ofprotists N for proteinsN for met when met bacterivores in plant in an an ) growth

added litter of high C:N ratioadded high ( of litter C:N ) increase concentration. inplant nutrient .

W ) . detritus of narrow C:nutrient ratiodetritus ofnarrow hen thereadily organic available C Plantago lanceolataPlantago Nutritional mechanisms C:N ratioC:N which likely was an excess energyanexpenditure

and

, stimulate

P for ribosomes and for energyP ribosomes a

s from consumed microbials from consumed will should prevail prevail should subsequent subsequent

compared tocontrols release nutrientsrelease for plant

bacterivores higher substantial plant substantial because deficiency microbes substantial root production root .

when nutrients By .

the excess by i.e. 13 . C

due to H and

- low labeling ere the release .

s is s is is 25

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decrease c symbionts or relatively belowground more photosynthates al. P highand NUEPUE U therefore may This null). plantsgrow case when insoils happen respectivecritical ratios distinguished four c and initiate importance to drive ofmechanisms during co microbe bacterivores The nutritional relativeand non dominance of between areobserved nutrientsavailable highly for when plants, rhizosphere due ratioplant C:N i.e. compared tocontrol. i Koller et al. ncreased rootarea surface onsumption of by microbes onsumption Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

nder such conditions, soil will bewill shifted

( plant biomass increased 2013a to greater nutrient availability substrates, C:N in low

d competition towards microbes -

) inoculation experiments microbial

cited allocate above, will nutrient thatlimitation demonstrates plants under

incorporated ( can along plotted be 2013a priming effectspriming or soil on might been have in favour of

and plants is low. is and plants ) ontrasting cases. In cases. caseontrasting

( C

found a found Mooshammer etMooshammer al.2014b I n contra UE Comment citer cedocument: ,

and substantially more . Plant ) microbes compared to shoot biomass (x1.3) intreatments (x1.3) bacterivores with compared biomass toshoot while substantially higher increase bacterivores

microbes byareand P N stronglylimited N and and P st to the LQ the st to treatment, s

a efficient resultphotosynthesis. ofa more

a soil will primarilywill from benefit the the (Figure

are strongly limited byare stronglylimited N and P nutrient concentration

ganic matter ( C: Kuzyakov and Xu2013 Kuzyakov

N will will (ii) 7 .B). and C: and 13 , thus providing energy, thus for 1 , plants - C fromC recent photosynthates. plant lead to lead nutritional mechanisms nutritional ) bacterivore

, and , T he term P .

stoichiometry status Under circumstances these the co

the plantratio C:N exhibit C:N and C:P ratios andexhibit C:N C:P above their consequently increase - i.e. gradient microbial biomass microbial biomass of root dominance -

effects when competition fo decreased

(the relative growth(the rate relative is d

) microbial

with . release likely to drivelikely to biomass (x1.8) biomass (x1.8) The experiment ofKollerThe et

on plants. on plants. the

high ra and C:N C:P and refers refers . induced by presenceof

competition for competition T d potential root

increased by 14% at thebeginningat or

his his

N expected toexhibit expected turnover At thesame time, and P to the in the plant relative This may be We We (i) r N ( and by relative plant and ly widerly and P

N and a - tios , 26

.

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 667 666 665 664 663 662 661 660 659 658 657 656 655 654 653 652 651 650 649 648 647 646 645 644 643

stoichiom numerous key ecosystem functions. In meta this 8. ( when happen response also cause an ofplant increase (or exhibit microbes according stoichiometric (co tospecies behavior availabilityroot architecture, and may below thecriticalratios. The presence of NUE and PUE intermediate nutrient but according to mechanisms above as described may for occur critical strongly by ratios; they arelimited orPaccording thus N tosoil bacterivores FennerLee and 1989 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Conclusion & Conclusion soils with low availability withlow soils oflabile

lateral root plants experience

low when plants grow in grow when plants mayalso

to are strongly limited byare strongly carbon limited etry

- bacterivores C:N and C:P andC:N C:P ratios. .

analysis,showed we that C In cases stress :N may

production

plant species plant species

Perspectives or occur ing ing decrease, C ; 2a :P Hanley and FennerHanley and1997 Comment citer cedocument: the role of the nutrient imb nutrient

(

(dominance ofnon ratios Ågren 2008 and b

iomass (dilution of plantnutrientconcentrationiomass (dilution can occur ( i.e. a 2b

while plants stoichiometric behavior relatively , respectively.

, plants root This may in happen C:N:P ratios in C:N:P

We alances surface ) . bacterivores

result C In cases

have C:N or C:P ratios belowtheir just or C:P have respective C:N

suggesttheoretical a (NUE (NUE nutrient ). bacterivores

Plant nutrientPlant concentrations arehigh enough to are limited byare their Pbut C:nutrientratios are N or limited -

which iscritical,which especiallyat early stages life nutritional mechanisms).nutritional This case area) for more efficient nutrient in Microbes and PUE and other both 3 ) - - . a and a dominance of mechanisms). Indominance case ofmechanisms). rich environment

soil

in

nutrient storageproduction and biomass substrates plant limiting soil contributedsoil significantly to , and thesu , microbial ,

3 become by carbon limited an b, plantsgrow insoils

are low expected tobe excessthe non uptake of framework framework

with low C:N and C:P ratios and C:N with low C:P

bsequent changes bsequent innutrient and plant

( nutrient concentration Jentschke et al.1995 Jentschke C:N:P based on based biomass uptake

with ratios ) is expectedto

and

and ecological -

limiting as in . plants )

4 Similar Similar , but their

, ) s, ,

or 27 ,

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 692 691 690 689 688 687 686 685 684 683 682 681 680 679 678 677 676 675 674 673 672 671 670 669 668

antagonistic interactionsbetween and and arenot protists nematodes quite common al. 2012 Also, ( et al.2004 It recognize is therhizosphere in them didit a plant(Figure of 1). species. investigated Only(15%) 6studies s average, ofstudiesused ofdifferentfound a wethat38% mixture Rhabditis and Clarholm2012 et al.1999 ha frequently hasa worldwide ubiquitous distribution usedit because model, corresponding28% of to focusingfound that57% ofstudies on bacteri tocommunityFrom population to various are environmental conditions inoculation experiments focusing on using meta yetgrowth. has Unfortunately, not ‘stoichiometric’ totestthis it possible been of Nandimmobilization P important Bonkowski 2012 andClarholm Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological s contribute

strongef biological among interactions bacteri vores vores ) . , Recent studies indicateRecent that intraguild studies

parameters ; ; Acrobeloides - analysis because tools ratios. insufficient and More onsoil plantC:N:P co data of Ronn etRonn al.2002 Kreuzeret fects on the activity ofthefectsthe composition microbial onsoil community and on ecosystemfunctions usuallyoneIn meta modelspecies. used this to d

our understanding that theeffects of ) . Concerning bacterial driving

al. 2006 al. Comment citer cedocument:

(and several other in ) , soil N , soil

bacterivore the bacterial biomass ; - level experimentslevel ; Rosenberg et al.2009 all studiesreported inthe meta Cheng et al.2011 bacterivores of

bacterivore mineralization bacterivore functions bacterivore functions therefore protists protists - effects - vores feeding nemat Cephalobidae oil oil

effects selectedthe on microbial communityon composition protists protists needed. - -

predation be predation are effects on –

, ;

St ( and plant soil Nand availability soil P Irshad et al.2011 diverse Ferris etal. 1998 udies investigating effects the of )

and nematodes together and 2of only and In

on plant

odes, the generaodes, the genera addition, in terrestrial ecosystem on

and tween tween responses in root architecture - analysis. Thisspeciesanalysis. was ), often antagonistic often nutrient acquisition in nutrient acquisition

protists protists A. were frequentlywere used. ( ‘ Geisen etGeisen al.2014 w

bacterivores’, especially castellanii e propose ) )

arespecies or p or Mesodiplogaster or nematodes nutrition a nutrition lant performance

for plants

hypothesis

three ( species as a Bonkowski Bonkowski - - analysis, we s specific ( . ( Griffiths Griffiths

Ronn etRonn

( nd outlooks outlooks ) Djigal ,

and On . ,

28 -

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 717 716 715 714 713 712 711 710 709 708 707 706 705 704 703 702 701 700 699 698 697 696 695 694 693

contrasting Nand soil Ac Inghaminstance,et al. and persistence of sequence of ofview.point growth orreplicates requires a nutrition number high of growth. Kinetic experiments are scarcebecau studies investigatedeffect the of experimentsKinetic monitor to predicting the bacterivore dissimilarityIdentifying dissimilarity (Rao’s coefficient). morphology, feeding types, keystone( species such as (i)species number of attribute(s) drive(s) theoverall effect of 2012 on ecosystem function has Unfortunately,of withineffect the increase 2008 Ronn Bonkowski etal. 2000 unidirectional. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological robeloides ) . Asa on community attributescommunity ;

communit

the consequence, we far areconsequence, still from predicting Neidig2010 et al. plant

sp.)

actual effects ofbacterialactual effects However Bacterivore cost

on plant and microbial e.g. Acanthamoebacastellanii bacterivore richness of other of other ies ; P ( Comment citer cedocument: , this typethis , of Neidiget al.2010 1985 availability wouldbe driving function ecosystem

( , (ii)keystonegroupswith specific ( ecology rarely nematodes

Bouteloua g body another another )

- ) observeda effect . The population densityof bacterivore r might potentially bacterivores esponses been investi been size, size, - trophic

s stud bacterivore

on ecosystemfunctions are known to preyare known on demographic paramdemographic

racilis the bacterivores ies ; temporary

group in the presence of Ronn - bacterivore induce might might

se monitoringse gated on plant performanceaftera ofon plant specific period ) optimal optimal growth ), (iv) particular trait dissimilarity (

( et al.2012 diversity ofthe soil Anderson and Coleman 1981 drive the d provide (

Postma

effects performanceplant on s effect ofnematodes( in the fields.

should helpshould to us to test the .

, community f onecosystem K

which is which inetic experiments conducted the most relevant relevant the most

one eters; eters; crucial ) - bacterivore bacterivore

Blaauw et al.2005 protists and vice bacterivores ( bacterivore Kromeal. 2009a et bacterivore etc.) (v)multi or stoichiometric

difficult information ( bacterivore - etAnderson al.1978 versa versa -

e.g. get commu effects , Pelodera

from a technicalfrom and and taxon

closer to amoebae), (iii) attributes community ( Bjornlund andBjornlund

) the dynamic on on plant ; nityeffects, . hypothesis.

Saleem etal. can thus community - – ) the trait unctions . For . For

head head sp. and Most

of soil

under under ;

. 29 A

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We thank We Acknowledg ecosystem services functions interactions deeply should understandingimprove our ecosystem functions. onbacteria Conducting morestudies detailed rhizosphere (pH, carbon texture, content, water content;plant species etc.), or cultivar, tote wasit impossible for eachlow factortoo was aftertime inoculation 2008 or cultivars ( factors are likelyto impact at the soil radio based onbiological interactions aand Thisis serious planttissues. deficiency Hinsingeret al.2011 and theveryconcentration thesoilsolution in ofavailable its low form in many environme E Chenget al.2011 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological mphasize onPandecologicalfactors ; - isotopes is probablyisotopes is waythe best tobetter how understand Irshad et al.2012 , -

Claire Marsdenfor providing help and plant interface.

( organisms ( Somasundaram etal. 2008 e ments ultimatelyhelpto us ; nts. In contrast N, nts. to in Ferris et al.1997 Ferris

) . Here, we found that N was 2.3 . Here, found we thatNwas ( the future.the st the effect of Krome etKrome al.2009a ) Comment citer cedocument: e.g.

or other free fauna Also, the literature that a indicates bacterivore

or difficult toaggregate mycorrhizal fungi between

predict how

) initial initial , soil p , soil - ) effects – , the presence of symbiotic mutualists , thepresence ofsymbiotic mutualists P ischaracterizedP by

plant roots and roots plant P isessentialP for may plantgrowth and limiting be ) , etc. Unfortunately,of observations thenumber bacterivore ( roperties ful comments on an on earlierful comments of review this draft Bonkowski andBonkowski Schaefer 1997 given

on ecosystem functions:on or or the erosion ofthe rhizobia that plant P acquisition that plantP efficiency to perform - ( times more studied than P in both soil moretimes bothsoil studiedthanPin Ekelund andRonn1994 of

biomass rhizosphere soil foodroles web soil ) on

lar its its bacterivore soil biod soil a ge

( relative immobility in bacterivores meta or density number of number / root

organisms. organisms. - analysis. instance, For iversity will /bacterivore bacterivore ( Hinsinge - induced e induced or ) ; , soil properties, soil

in Tao et al.2009

the presence of other affect cycling P ( ) Herdleret al. , plantspecies ecosystems Using P r 2001

species species ecological ffects on ffects affect is soil soil

; oft . en

) 30 , ,

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Anderson ET,McClellan CV,Hunt Coleman JF, DC, Cole HW RV,Elliott (1978) Trophic AndersonDC (1981) development Population RV,Coleman andinteractions between 2 L,InghamAnderson Woods R,GouldW, Coleman Organic D(1983) CambardellaR, and C, Bonkowski M,Scheu(1996)Alphei Nematoda S Protozoa, J, Lumbricidae inthe and Ågren GI Agren stoichiomestry(2004) C:N:P GIThe autotrophs of AG, Lane Simpson Adl SM, Lukeš Bass Bow CE, J, D, AG, Farmer Simpson Adl SM, Andersen Anderson RA, MA, OR, References Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological rhizosphere of review andsystematics:ecology, of evolution, 153 7: 185 Eukaryotic 59:429 Microbiology Dunthorn M,Hampl The V(2012) of classification revised eukaryotes. of Journal Microbiology 52:399 eukaryotes onthetaxonomy ofEukaryotic withemphasis Journal ofprotists. BrugerolleFensome FredericqRA, G, The (2005)of newlevel S higher classification of bacteria,nematodes. amebas,361 and Microb4: Ecol interactions i species nematodes. of Nematologica bacteriophagic 27:6 inorganic by nitrogenousinso nematodes losses microbivorous microorganisms andplant growth. effectson Oecologia 106:111

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Comment citer cedocument: - 437.

7) C: N: P stoichiometry7) C:N:P there is “Redfield ratio” insoil: a for LiBS, Li HXF, (2011) Stimulatoryeffects DM,Hu of

- 380. zal fungus Glomus mosseae. Plant Plant fungusmosseae.zal Glomus

- 252. - - 309. 187. sformations. Microb Ecolsformations. 381 4: Microb

- saprophage interactions in in interactions saprophage

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Yeates asNematodes indicators: (2003) soil functional GW andbiodiversityBiologyaspects. Yeates(2007) Abundan G (2013) carbon, AglobalXu X, WM analysis Post Thornton ofsoilmicrobial PE, biomass XiaoLiu JG, HF,Li HuF,Influence XY, B, Griffiths MQ,Jiao Chen HX(2010) ofbacterial (1975) EliminationWright DJ by of nitrogenous compounds Weisse T(2002) inter The significance of VogelsWeekers(1993) Effects PH, BodelierJP, PL,GD Wijen o Wallenda (1999) T,Read Kinetics DJ of aminouptakeroots.Plant acid by ectomycorrhizal DH Wall Wagg F,MGA Bender (2014)and C, Widmer derbiodiversity Soil soil SF, Heijden van Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comparative Biochemistry 52:247 1945 (Nematoda: Cephalobidae).Co Molecular81: 327 Microbiology herbivorousLeeuwenhoek AntonieInternational Van protists. and ofGeneral Journal vermiformis amoebaesoil Acanthamoebacastellanii, Environ22:179 Cell National Academy Of Of America Sciences OfUnitedStates 111:5266 The community determine composition ecosystem multifunctionality. ProceedingsThe Of and Fertility199 37: ofSoils Canadiansoils. journal offorest research37:216 22: 737 nitrogenin terrestrialand phosphorus GlobalEcologyBiogeography ecosystems. and commun feeding onnitrificationammonia nematodes and the , Bardgett Kelly RD, Biodiversity (2010) EF Nat inthe297 dark. 3: Geosci - 749. ity Ecology Applied131 composition. Soil 45:

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Zwart (1992)and Growth nitrogenous KB, Darbyshireexcre JF Zechmeis Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological 157. flagellate organicsoil transformations. matter (2015)J, Wanekapplication Thestoichiometry W of ecological toplant ter

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Table 1. Table $ * Mean Ranoarisoaal. et Kolleral. et Irshadal. et Chengal. et Irshadal. et Kromeal. et Herdleral. et al.Kreuzer et BonkowskiBrandt & Bonkowskial. et al.Jentschke et References Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Numberof tips estimated from number of roots Specificroot length (SRL)

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Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: Click heretodownloadlinefigure:Figure1.docx line figure1 Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 Figure 1. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Protists Nematodes + Mycorrhizal fungi Rhizospheric soil Criteria Annual plant Woody plant Phosphorus Nematodes Number of studies includedNumber inthemeta of studies Nitrogen Protists Total 0 Comment citer cedocument: 5

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Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6

Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: Click heretodownloadlinefigure:Figure2.docx line figure2 Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 :shoot:root ratio.S:R Q eachnumber of observationsfunction. for M the ES bars to95%confidenceHorizontal correspond intervals. numbers above circles Bold specify circles (differentnon indicateand from significant zero) Figure 2. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological biomass mic Plant Plant N Plant

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Click heretodownloadlinefigure:Figure4.docx line figure4 Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 P significantES difference in protists Nconcentrationroot biomass (B) (C)and according shoot bacterial tothe presenceof Figure 4. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological <0.05. ES ES m m

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observations). byexplanatory and each by their variable variables).% variable) ES as of a function Nconcentrationshoot (explanatory ES variables). (B) total N Figure 5. Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

B ES on A ES on total P amount i i total N amount in shoot

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of Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6

Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: Click heretodownloadlinefigure:Figure6.docx line figure6 Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 6 5 4 3 2 1

Kruskal mycorrhizal plant). Different letters (aand biomass accordingpresence to the ofmycorrhizalfungi ( Figure 6 Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ES m - 0.2 Wallis test( Wallis 0.1 . Changes in . Changes A 0 Shoot Shoot Mycorrhizal Mycorrhizal - P a M bacterivore <0.05, n=14). <0.05, biomass Comment citer cedocument: +M - a b status induced effect size (mean) root effectsize and (B)induced on (A) shoot

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Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: Click heretodownloadlinefigure:Figure7.docx line figure7 Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 11 10 9 8 7 6 5 4 3 2 1

given momentinthe experiment. grad changes. C:N the describe of presence the in behavior plant of cases different four illustrating Diagram (B) function rate. of relativegrowth We here defined the C:limiting Relationship (A) effects 7. Figure Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological ient. *the term “dominance” describes the relative importance of mechanisms to initiate and drive the effects of effects the drive and initiate to mechanisms of importance relative the describes “dominance” term *the ient.

on plantperformance. Grey arrows describe the hypothetical hypothetical the describe arrows Grey

- hoeia faeok eciig h rltv dmnne o ntiinl n non and nutritional of dominance* relative the describing framework Theoretical nutrient (N o nutrient (N cri ewe pat eaie rwh ae n pat :uret ais mdfe fo Ågren from (modified ratios C:nutrient plant and rate growth relative plant between

and C:P and Comment citer cedocument: r P) ratio while the broken lines indicate three different variations in the C:nutrient ratio of a second element (N or P) as orP) (N element second a ratio of theC:nutrient variations different in lines indicate three ratiothebroken P) while r cri

according to soil C:N:P ratio, while the broken line indicates a hypothetical zone where the dominant mechanism dominant the where zone hypothetical a indicates line broken the while ratio, C:N:P soil to according

trends in microbial nitrogen microbial in trends critical

C:limiting - nutrient ratio (R nutrient -

and phosphorus and bacterivores cri ) above the relativegrowth which - - use efficiency (NUE, PUE) (NUE, efficiency use urtoa mcaim ivle in involved mechanisms nutritional

along a soil soil a along ( 2008 C:N ) the describes line solid The ). and and bacterivores C:P

gradients. Solid lines Solid gradients. rate isnull. rate along the soil C:N:P soil the along

on plants at a a at plants on bacterivore

a - Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 13 12

Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological R cri Plant C:nutient ratios A 2 1 Second Second Excess nutrient Relative Relative uptake Comment citer cedocument: 3 3 growth

rate Max 4

Substrate C:P ratio B Plant C:P Plant 3b 2b 4 non Dominance Dominance of cri pathways - nutritional Substrate C:N ratio C:N Substrate Microbial NUEMicrobial Dominance Dominance of nutritional nutritional pathways 3a

Plant C:Ncri 2a 1

Micobial PUE

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6

Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: Supplementary Material Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 1

Appendix 1. Appendix Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological

List ofstudies(in chronological order) used inthe meta Comment citer cedocument:

- analysis.

Version postprint importance ofsoilbacterivores forecosystem functions. Plantand Soil,1-24.DOI :10.1007/s11104-015-2671-6 2

Irshad et al. et Irshad al. et Cheng Xiaoal. et Krome al. et Krome al. et Ekelund al. et al. et Somasundaram Herdler al. et Postma-Blaauw al. et Djigal al. et Djigal al. et Bonkowskial. et Bonkowskial. et Bonkowskial. et & Chan Bardgett al. Setälä et Ferrisal. et al. et Alphei al. et Jentschke Bouwman al. et al. et Rutherford Kuikman al. et al. Setälä et Kuikman al. et Kuikman & Van Veen Griffiths al. Ingham et Clarholm al. et Anderson Trofymow al. et al. et Woods al. et Baath al. et Anderson Cole al. et Elliott al. et Cole al. et Coleman al. et References Ranoarisoa et al. et Ranoarisoa Koller al. et Koller al. et al. et Irshad al. Bjornlund et Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological 2015 2013b 2013a 2012 2012 2011 2011 2010 2009b 2009a 2009 2008 2008 2005 2004b 2004a 2001b 2001a 2000 1999 1999 1998 1996 1995 1994 1992 1991 1991 1990 1989 1986 1985 1985 1983 1983 1982 1981 1981 1978 1979 1978 1977 Year France Germany Germany France Denmark France China China Germany Germany Netherlands Japan Germany Netherlands Senegal Senegal Germany UK UK UK Finland USA Germany Germany Netherlands Canada Netherlands Finland Netherlands Netherlands Scotland USA Sweden USA USA USA Sweden USA USA USA USA USA Country Comment citer cedocument: Soil-sand mixtureSoil-sand mixtureSoil-sand mixtureSoil-sand Agar Soil-OM mixture Agar Soil Soil-OM mixture Agar/Sand mixtureSand-OM Soil-OM mixture Soil Soil Soil-OM mixture Soil Soil Humus substrate Soil-sand-OM substrate Soil-sand-OM Soil substrate Sand-OM substrate Sand-OM Soil solution + nutrient Sand Soil Soil Soil Humus Soil Soil Soil Soil Soil Soil Soil Soil Humus Soil Soil Soil Soil Soil Medium

No Yes Yes No No No No No Yes Yes Yes Yes Yes No No No Yes Yes Yes No No No Yes Yes No Yes Yes No Yes Yes Yes No Yes No No Yes No No Yes Yes Yes Yes Protist Bacterivores Yes No No Yes Yes Yes Yes Yes No No No No No Yes Yes Yes No No Yes Yes Yes Yes Yes No Yes No No Yes No No Yes Yes No Yes Yes Yes Yes Yes Yes No Yes Yes Nematode Yes Yes Yes No Yes Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes No Yes Nitrogen Nutrients Yes No No Yes No Yes No No No No No No Yes No Yes Yes Yes Yes No Yes No No Yes Yes No No No Yes No No Yes Yes No No No No No Yes Yes Yes Yes Yes Phosphorus Pinus pinaster Pinus lanceolata Plantago lanceolata Plantago pinaster Pinus vulgare Hordeum pinaster Pinus Oryza sativa No thaliana Arabidopsis & sativum Lepidium thaliana Arabidopsis lanatus Holcus Oryza sativa Oryza sativa No mays Zea mays Zea abies Picea aestivum Triticum perenne Lolium stricta Nardus sylvestris Pinus No europaeus Hordelymus abies Picea No No aestivum Triticum No aestivum Triticum aestivum Triticum No gracilis Bouteloua sp. Triticum No No No sylvestris Pinus No No No No No Plant (species) Yes No Yes Yes No No No No No No No No Yes No No No Yes No No No Yes No No Yes No No No No No No No No No No No No No No No No No No Mycorrhiza Personnal communication Personnal Ecology Microbiology FEMS Biochemistry & Biology Soil Soil and Plant Biology of Soil Journal European Biochemistry & Biology Soil Nematology Ecology Soil Applied Soil & Plant Biochemistry & Biology Soil Biochemistry & Biology Soil Science Production Plant Biochemistry & Biology Soil Oecologia Biochemistry & Biology Soil Soil & Plant Ecology Soil Applied Oïkos Ecology Soil Applied Biochemistry & Biology Soil Oïkos Soil and Plant Oecologia of Soils Fertility and Biology of Soils Fertility and Biology Science of Soil Journal Canadian Biochemistry & Biology Soil Pedobiologia of Soils Fertility and Biology of Soils Fertility and Biology Biochemistry & Biology Soil Monographs Ecological Biochemistry & Biology Soil Oïkos Oecologia Biochemistry & Biology Soil Oïkos Ecology Microbial Ecology Microbial Studies J. Environmental Intern. Ecology Microbial Bulletins Ecological Journals

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Trap, J., Bonkowski,M., Plassard,C., Villenave,C., Blanchart,E. (2015). Ecological Comment citer cedocument: