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Co-Occurrence of Rhizobacteria with Nitrogen Fixation And/Or 1

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Co-Occurrence of Rhizobacteria with Nitrogen Fixation And/Or 1 Co-occurrence of rhizobacteria with nitrogen fixation and/or 1-aminocyclopropane-1-carboxylate deamination abilities in the maize rhizosphere Sébastien Renoud, Marie-Lara Bouffaud, Audrey Dubost, Claire Prigent-Combaret, Laurent Legendre, Yvan Moenne-Loccoz, Daniel Muller To cite this version: Sébastien Renoud, Marie-Lara Bouffaud, Audrey Dubost, Claire Prigent-Combaret, Laurent Leg- endre, et al.. Co-occurrence of rhizobacteria with nitrogen fixation and/or 1-aminocyclopropane- 1-carboxylate deamination abilities in the maize rhizosphere. FEMS Microbiology Ecology, Wiley- Blackwell, 2020, 96 (5), 10.1093/femsec/fiaa062. hal-02547931 HAL Id: hal-02547931 https://hal-univ-lyon1.archives-ouvertes.fr/hal-02547931 Submitted on 24 Nov 2020 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. Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License FEMS Microbiology Ecology http://mc.manuscriptcentral.com/fems Co-occurrence of rhizobacteria with nitrogen fixation and/or 1-aminocyclopropane-1-carboxylate deamination abilities in the maize rhizosphere Journal: FEMS Microbiology Ecology ManuscriptFor ID FEMSEC-20-01-0023.R2 Peer Review Manuscript Type: Research article Date Submitted by the n/a Author: Complete List of Authors: Renoud, Sébastien; Université de Lyon, Université Claude Bernard Lyon 1 UMR5557 Bouffaud, Marie-Lara; Université de Lyon, UMR CNRS 5557 Ecologie Microbienne Dubost, Audrey; Universite Claude Bernard Lyon 1 Faculte des Sciences et Technologies, UMR 5557 Microbial Ecology Laboratory Prigent-Combaret, Claire; Université de Lyon, UMR CNRS 5557 Ecologie Microbienne Legendre, Laurent; Université de Lyon, UMR5557 Moënne-Loccoz, Yvan; Université de Lyon, UMR CNRS 5557 Ecologie Microbienne Muller, Daniel; Université de Lyon, UMR5557 microbiota, plant growth promotion, functional group, functional Keywords: microbiota, holobiont, ITSNTS theory ScholarOne Support 1-434/964-4100 Page 1 of 84 FEMS Microbiology Ecology 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 For Peer Review 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 395x318mm (72 x 72 DPI) 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 ScholarOne Support 1-434/964-4100 FEMS Microbiology Ecology Page 2 of 84 1 2 3 1 Co-occurrence of rhizobacteria with nitrogen fixation and/or 1-aminocyclopropane-1- 4 5 6 2 carboxylate deamination abilities in the maize rhizosphere 7 8 3 9 10 4 11 12 5 13 14 1‡ 1‡ 1 1 15 6 Sébastien Renoud , Marie-Lara Bouffaud , Audrey Dubost , Claire Prigent-Combaret , 16 17 7 Laurent Legendre1,2, Yvan Moënne-Loccoz1 and Daniel Muller1* 18 19 8 20 21 For Peer Review 1 22 9 Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR5557 23 24 10 Ecologie Microbienne, 43 bd du 11 novembre 1918, F-69622 Villeurbanne, France 25 26 11 2 Univ Lyon, Université de St Etienne, F-42000 St Etienne, France 27 28 29 12 30 31 13 ‡ Current addresses: 32 33 14 S.R. : BGene genetics Bâtiment B Biologie, F-38400 Saint Martin d'Hères, France 34 35 15 M.L.B. : Helmholtz Center for Environmental Research UFZ, Theodor-Lieser-Straβe 4, 36 37 38 16 06120 Halle, Germany 39 40 17 41 42 18 43 44 45 19 Running title: nifH and acdS bacteria on maize 46 47 20 48 49 21 50 51 52 22 *Corresponding author: UMR CNRS 5557 Ecologie Microbienne, Université Lyon 1, 43 bd 53 54 23 du 11 Novembre 1918, 69622 Villeurbanne cedex, France. Phone: +33 4 72 43 27 14. E-mail: 55 56 24 [email protected] 57 58 25 59 60 1 ScholarOne Support 1-434/964-4100 Page 3 of 84 FEMS Microbiology Ecology 1 2 3 26 ABSTRACT 4 5 6 27 7 8 28 The plant microbiota may differ depending on soil type, but these microbiota probably share 9 10 29 the same functions necessary for holobiont fitness. Thus, we tested the hypothesis that 11 12 30 phytostimulatory microbial functional groups are likely to co-occur in the rhizosphere, using 13 14 15 31 groups corresponding to nitrogen fixation (nifH) and 1-aminocyclopropane-1-carboxylate 16 17 32 deamination (acdS), i.e. two key modes of action in plant-beneficial rhizobacteria. The analysis 18 19 33 of three maize fields in two consecutive years showed that quantitative PCR numbers of nifH 20 21 For Peer Review 22 34 and of acdS alleles differed according to field site, but a positive correlation was found overall 23 24 35 when comparing nifH and acdS numbers. Metabarcoding analyses in the second year indicated 25 26 36 that the diversity level of acdS but not nifH rhizobacteria in the rhizosphere differed across 27 28 29 37 fields. Furthermore, between-class analysis showed that the three sites differed from one 30 31 38 another based on nifH or acdS sequence data (or rrs data), and the bacterial genera contributing 32 33 39 most to field differentiation were not the same for the three bacterial groups. However, co- 34 35 40 inertia analysis indicated that the genetic structures of both functional groups and of the whole 36 37 38 41 bacterial community were similar across the three fields. Therefore, results point to co-selection 39 40 42 of rhizobacteria harboring nitrogen fixation and/or 1-aminocyclopropane-1-carboxylate 41 42 43 deamination abilities. 43 44 45 44 46 47 45 Keywords: microbiota; phytostimulation; functional group; functional microbiota; holobiont; 48 49 46 ITSNTS theory 50 51 52 47 53 54 48 55 56 57 58 59 60 2 ScholarOne Support 1-434/964-4100 FEMS Microbiology Ecology Page 4 of 84 1 2 3 49 INTRODUCTION 4 5 6 50 7 8 51 Plant Growth-Promoting Rhizobacteria (PGPR) colonize plant roots and implement a range of 9 10 52 plant-beneficial traits, which may result in enhanced plant development, nutrition, health and/or 11 12 53 stress tolerance (Almario et al. 2014; Cormier et al. 2016; Gamalero and Glick 2015; Hartman 13 14 15 54 et al. 2018; Vacheron et al. 2013). As a consequence, PGPR strains have received extensive 16 17 55 attention for use as microbial inoculants of crops (Bashan et al. 2014; Couillerot et al. 2013). 18 19 56 Plant-beneficial effects exhibited by PGPR are underpinned by a wide range of modes 20 21 For Peer Review 22 57 of actions, which include (i) enhanced nutrient availability via associative nitrogen fixation 23 24 58 (Puri et al. 2016, Deynze et al. 2018) or phosphate solubilization (Arruda et al. 2013), (ii) 25 26 59 stimulation of root system establishment through phytohormone synthesis (Cassán et al. 2014) 27 28 29 60 or consumption of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) via an 30 31 61 enzymatic deamination (Glick 2014), and (iii) the induction of systemic resistance responses in 32 33 62 plant (Pieterse and Van Wees 2015). In addition to phytostimulation, certain PGPR may also 34 35 63 achieve inhibition of phytoparasites using antimicrobial secondary metabolites (Agaras et al. 36 37 38 64 2015) or lytic enzymes (Pieterse and Van Wees 2015). Often, PGPR strains display more than 39 40 65 one phytostimulatory mode of action, which is considered important for effective plant- 41 42 66 beneficial effects (Bashan and de-Bashan 2010; Bruto et al. 2014; Rana et al. 2011; Vacheron 43 44 45 67 et al. 2017). Therefore, the co-occurrence of multiple phytostimulation traits is likely to have 46 47 68 been subjected to positive evolutionary selection in PGPR populations to maximize success of 48 49 69 the plant-PGPR cooperation. This hypothesis is substantiated by genome sequence analysis of 50 51 52 70 many prominent PGPR strains from contrasted taxa (Bertalan et al. 2009; Chen et al. 2007; 53 54 71 Redondo-Nieto et al. 2013; Wisniewski-Dyé et al. 2012). 55 56 72 Even though PGPR strains tend to accumulate several plant-beneficial traits (Bruto et 57 58 73 al. 2014), the co-occurrence patterns of these traits are not random. This takes place in part 59 60 3 ScholarOne Support 1-434/964-4100 Page 5 of 84 FEMS Microbiology Ecology 1 2 3 74 because many past horizontal gene transfers of the corresponding genes were ancient (Frapolli 4 5 6 75 et al. 2012), often leading to clade-specific profiles of plant-beneficial traits (Bruto et al. 2014). 7 8 76 However, the analysis of 304 proteobacterial genomes from contrasted taxa evidenced, overall, 9 10 77 the co-occurrence of nifHDK (nitrogen fixation) and acdS (ACC deamination) based on Exact- 11 12 78 Fisher pairwise tests (Bruto et al. 2014), raising the possibility that nitrogen fixation and ACC 13 14 15 79 deamination might be useful traits when combined in a bacterium. Indeed, nitrogen fixation and 16 17 80 ACC deamination occur together in various rhizobacteria (Blaha et al. 2006; Duan et al. 2009; 18 19 81 Jha et al. 2012; Ma, Guinel, and Glick, 2003; Nukui et al. 2006), but the relation between both 20 21 For Peer Review 22 82 traits can be complex. In Azospirillum lipoferum 4B for instance, the plasmid-borne gene acdS 23 24 83 is eliminated during phase variation while nif genes are maintained (Prigent-Combaret et al.
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