REVIEW ARTICLE published: 15 June 2012 doi: 10.3389/fmicb.2012.00210 Drivers of archaeal -oxidizing communities in soil

Kateryna Zhalnina1, Patrícia Dörr de Quadros2, Flavio A. O. Camargo2 and Eric W.Triplett1*

1 Microbiology and Cell Science Department, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, USA 2 Soil Science Department, Federal University of Rio Grande do Sul, Porto Alegre, Brazil

Edited by: Soil ammonia-oxidizing (AOA) are highly abundant and play an important role in Rich Boden, University of Plymouth, the . In addition, AOA have a significant impact on soil quality. pro- USA duced by AOA and further oxidized to nitrate can cause nitrogen loss from soils, surface Reviewed by: and groundwater contamination, and water eutrophication. The AOA discovered to date Jennifer F.Biddle, University of Delaware, USA are classified in the phylum . Only a few archaeal genomes are available J. Michael Beman, University of in databases. As a result, AOA are not well annotated, and it is difficult to mine California, Merced, USA and identify archaeal genes within metagenomic libraries. Nevertheless, 16S rRNA and Nathan Basiliko, University of Toronto, Canada comparative analysis of ammonia monooxygenase sequences show that soils can vary greatly in the relative abundance of AOA. In some soils, AOA can comprise more than 10% *Correspondence: Eric W. Triplett, Department of of the total prokaryotic community. In other soils, AOA comprise less than 0.5% of the Microbiology and Cell Science, community. Many approaches have been used to measure the abundance and diversity of Institute of Food and Agricultural this group including DGGE, T-RFLP,q-PCR, and DNA sequencing. AOA have been studied Sciences, University of Florida, 1052 Museum Road, Gainesville, across different soil types and various from the Antarctic dry valleys to the FL 32611-0700, USA. tropical forests of South America to the soils near Mount Everest. Different studies have e-mail: ewt@ufl.edu identified multiple soil factors that trigger the abundance of AOA.These factors include pH, concentration of available ammonia, organic matter content, moisture content, nitrogen content, clay content, as well as other triggers. Land use management appears to have a major effect on the abundance of AOA in soil, which may be the result of nitrogen fertilizer used in agricultural soils. This review summarizes the published results on this topic and suggests future work that will increase our understanding of how soil management and View metadata, citation and similar papers at core.ac.uk brought to you by CORE edaphoclimatic factors influence AOA. provided by PubMed Central Keywords: ammonia-oxidizing archaea, ammonia monooxygenase, soil

DISCOVERY OF THE AMMONIA-OXIDIZING ARCHAEA, THEIR aerobically oxidizing ammonia to nitrite. Wuchter et al. (2006) , PHYSIOLOGY, AND enriched a crenarchaeote from North Sea water and showed that its FIRST DISCOVERIES OF NOVEL GROUP abundance, but not the abundance of AOB, correlates with ammo- Chemolithotrophic nitrification is a two-step process. First step nium oxidation to nitrite. The same study also found that archaeal includes oxidation of ammonia to nitrite conducted by ammonia- amoA copy numbers were higher than bacterial amoA. Since the oxidizing bacteria (AOB) and second step is conversion of nitrite early work on , multiple studies have observed a to nitrate by nitrite-oxidizing bacteria (NOB; Hastings et al., 2000; predominance of AOA over AOB in multiple environments, par- Hermansson and Lindgren, 2001; Kowalchuk and Stephen, 2001). ticularly in soil (Leininger et al., 2006; Nicol et al., 2008; Schauss Before the discovery of large numbers of ammonia-oxidizing et al., 2009; Zhang et al., 2010). archaea (AOA) in the environment, aerobic ammonia-oxidizers were thought to be restricted to AOB from β- and γ-subclasses CLASSIFICATION: THAUMARCHAEOTA OR CRENARCHAEOTA? of the Proteobacteria. The first published evidence that archaea Initially, AOA were classified as mesophilic Crenarchaeota might be involved in ammonia oxidation came from the discovery (Treusch et al., 2005). Brochier-Armanet et al. (2008) proposed of archaeal homologs to bacterial ammonia monooxygenase that the archaeal ammonia oxidizers were sufficiently distinct to (amoA) in archaea-associated scaffolds from the whole genome be separated from the Crenarchaeota into a new phylum, Thau- shotgun sequencing project of the Sargasso Sea (Venter et al., marchaeota. This distinction was based on phylogenetic analysis 2004). An in silico comparison to environmental sequences from of ribosomal encoding genes and some protein-coding public databases revealed that the archaeal amoA and amoB genes genes. Comparative phylogenetic analysis of marine and soil AOA from the large-insert environmental fosmid library of a calcare- revealed six conserved signature indels and more than 250 pro- ous grassland were highly similar to archaea-associated scaffolds teins unique only to the Thaumarchaeota (Spang et al., 2010). from the Sargasso Sea (Treusch et al., 2005). This insert also con- Also, Pelve et al. (2011) found that the Cdv system, related to tained a 16S rRNA gene that proved that the organism from the eukaryotic ESCRT-III machinery, is the primary cell division which this amoA homolog originated was a mesophilic Crenar- system in the thaumarchaeon maritimus and that chaeota. At the same time, Könneke et al. (2005) isolated a marine the FtsZ protein performs a function in archaea other than cell crenarchaeote (SCM1) that grows chemolithoautotrophically by division.

www.frontiersin.org June 2012 | Volume 3 | Article 210 | 1

“fmicb-03-00210” — 2012/6/13 — 21:04 — page1—#1 Zhalnina et al. Drivers of AOA in soils

ECOPHYSIOLOGY has been difficult. The lack of a variety of cultured AOA and Ammonia-oxidizing archaea and AOB oxidize ammonia by using AOA genomes has limited the study of their physiology and ammonia monooxygenase (AMO) enzyme. Although nitrite is metabolism. the final product for both archaeal and bacterial ammonia oxida- tion, big differences exist between the AOA and AOB ammonia ECOLOGICAL ROLE OF AOA AND WHY STUDY THEM? oxidation processes. First, the intermediate product of bacterial First, AOA are likely involved in nitrate leaching from soils, which ammonia oxidation to nitrite is hydroxylamine (Kowalchuk and causes surface and groundwater contamination. Nitrogen loss can Stephen, 2001). The intermediate product of archaeal ammo- occur at many points during the nitrification process (Kowalchuk nia oxidation is not as clear, but nitroxyl has been proposed as and Stephen, 2001). The nitrate produced during nitrification the intermediate (Walker et al., 2010). Second, the structure of can lead to the elimination of fixed nitrogen from an environ- AMO differs between bacteria and archaea (Könneke et al., 2005; mental system. Nitrate leaching from soil is another important route of nitrogen loss from ecosystems. Cationic ammonium Walker et al., 2010). Third, archaeal AMO has a higher affin- + (NH4 ) molecules are more stable in soil through binding to ity for substrate than does bacterial AMO (Martens-Habbena − et al., 2009; Martens-Habbena and Stahl, 2011). Fourth, while anionic soil particles, but nitrate (NO3 ) has more mobility in soil AOB are obligate autotrophs, AOA can also use organic carbon and can easily leach from the soil surface to groundwater causing (Hallam et al., 2006; Walker et al., 2010; Blainey et al., 2011; Tourna contamination (Kowalchuk and Stephen, 2001). et al., 2011). Differences listed above between AOA and AOB Second, AOA activity may be a significant source of green- led to the idea of existence of different physiological approaches house gas emissions from the soil. Recently, it was found that in utilizing of available nutrient resources between these two nitrous oxide (N2O) is the dominant ozone-depleting substance groups. emitted in the 21st century (Ravishankara et al., 2011). Nitrous oxide is transported to the stratosphere where it destroys ozone DIFFICULTIES IN STUDYING AOA: CULTIVATION, LACK OF through a nitrogen oxide-catalyzed process. Nitrous oxide has REFERENCE GENOMES 298 times higher global warming potential than carbon dioxide To date, only eight AOA have been described from marine, (CO2; van Groenigen et al., 2011). Autotrophic nitrification is a soil, sediment, and hot spring environments (Table 1). Two main pathway of nitrous oxide production in soil environments of them were isolated in pure cultures, and five species can (Colliver and Stephenson, 2000; Kowalchuk and Stephen, 2001; grow in enriched cultures but were not isolated in pure cul- Shaw et al., 2006). Santoro et al. (2011) suggested that AOA may tures. Only six whole genomes of AOA are available in the be largely responsible for the nitrous oxide production in marine databases. As the AOA have been found under a wide variety of environments. As AOA outnumber AOB in soil, it is possible that conditions including varied temperature, pH, ammonia concen- archaea may be the major source of soil nitrous oxide emission. trations, and oxygen supply, designing media for their cultivation Jung et al. (2011) observed that production of nitrous oxide by the

Table 1 | Ammonia-oxidizing archaea isolated from different environments.

# AOA Environment Source of isolation Classifi- Culture Genome Reference Country cation sequence

1 Nitrosopumilus Marine Gravel from a marine 1.1a Pure + Könneke et al. (2005),USA maritimus tropical fish tank Walker et al. (2010) 2 Cenarchaeum Marine symbiont Marine sponge 1.1a – + Preston et al. (1996),USA symbiosum Axinellamexicana Hallam et al. (2006) 3 Ca. Soil, hot springs Enrichment cultures from 1.1b Enriched + Hatzenpichler et al. (2008) Austria gargensis microbial mats of the Siberian Garga hot spring 4 Nitrososphaera Soil Garden soil in Vienna, Austria 1.1b Pure + Tourna et al. (2011) Austria viennensis 5 Ca. Nitrosoarchaeum Rhizosphere Soil sample from the rhizosphere 1.1a Enriched + Kim et al. (2011), Republic koreensis of Caraganasinica Jung et al. (2011) of Korea 6 Ca. Nitrosoarchaeum Sediments Sediments in the low-salinity 1.1a Enriched + Blainey et al. (2011) USA limina region of San Francisco Bay 7 Ca. Nitrosocaldus Hot springs Yellowstone National Park, ThAOA Enriched − de la Torre et al. (2008) USA yellowstonii hot springs 8 Ca. Nitrosotalea Soil Acidic agricultural soil 1.1a- Enriched − Lehtovirta-Morley et al. UK devanaterra associated (2011)

Frontiers in Microbiology | Terrestrial Microbiology June 2012 | Volume 3 | Article 210 | 2

“fmicb-03-00210” — 2012/6/13 — 21:04 — page2—#2 Zhalnina et al. Drivers of AOA in soils

soil archaeon Ca. Nitrosoarchaeum koreensis and rates of nitrous affinity of AOB (Martens-Habbena et al., 2009; Martens-Habbena oxide production are dependent on soil ammonia and dissolved and Stahl, 2011). These microorganisms can obtain energy even oxygen (DO) concentration. To date, the mechanism of nitrous under very low concentrations of substrate. It has been suggested oxide production by archaea is unclear. that the differences in substrate affinities allow AOA and AOB Possible consequences of autotrophic nitrification are contami- to inhabit distinct niches separated by substrate concentration nation of surface and ground water, loss of soil fertility, emission of and thereby reduce competition (Martens-Habbena et al., 2009; greenhouse gases, and chemical degradation of agricultural lands Schleper, 2010; Martens-Habbena and Stahl, 2011; Verhamme (Oldeman et al., 1991; Kowalchuk and Stephen, 2001; Ghosh and et al., 2011). There are studies that suggest substrate inhibition Dhyani, 2005; Santoro et al., 2011). AOA are frequently dominant of archaeal nitrification if high concentrations of ammonia are ammonia oxidizers in soils (Leininger et al., 2006), and, there- present (Di et al., 2010; Tourna et al., 2010). fore, their activity could lead to these consequences. Studying Because AMO in AOA has a much higher affinity for sub- the abundance and composition of archaeal ammonia oxidiz- strate than the analogous process in AOB, it has been suggested ers and understanding how soil properties influence this group that AOA dominate over AOB where ammonia concentrations are has long-lasting implications for sustainable agriculture and it particularly low. This seems to be the case in oligotrophic envi- attracts the attention of many research groups from around ronments such as sea water or hot springs (Hatzenpichler et al., the world. 2008; Walker et al., 2010). For example, Ca. Nitrososphaera gar- gensis, which was first found in hot springs, fixes bicarbonate at EDAPHOCLIMATIC FACTORS THAT MAY INFLUENCE AOA lower levels when the ammonia concentration was higher than ABUNDANCE AND DIVERSITY 3.1 mM. The optimal ammonia concentration for bicarbonate Main environmental factors that shape the ecological niches of fixation was much lower, between 0.14 and 0.8 mM (Hatzenpich- AOA from the ocean, hot springs, soils, and sediments were ler et al., 2008). Some studies suggest that substrate concentration discussed in the review paper by Erguder et al. (2009).Recent does not influence thaumarchaeal ammonia oxidation (Stopnisek advances in ecology, genetics, physiology, and culturing hap- et al., 2010; Verhamme et al., 2011). These authors showed that pened in the field of AOA, such as sequencing of first genome AOA grew similarly at low, medium, and high ammonia con- of non-symbiotic marine AOA (Walker et al., 2010), obtaining centrations, whereas AOB grew best only with high ammonia pure cultures, and high enrichments of Nitrososphaera viennensis concentrations. Other factors were suggested to be important in (Tourna et al.,2011), Ca. Nitrosoarchaeum koreensis, Ca. Nitrosoar- the growth of AOA. Di et al. (2009) observed in nitrogen-rich chaeum limina, Ca. Nitrosotalea devanaterra and sequencing of grassland soils neither AOA abundance nor their activity increased their genome; discovery of AOA ecotypes in soils based on differ- with the application of a large dose of ammonia substrate. In this entpHlevels(Gubry-Rangin et al., 2011) and another evidences study, AOA abundance was not quantitatively related to nitrifica- of organic carbon utilization provided more information about tion rates. Similarly, Ke and Lu (2012) did not see any changes physiology and metabolism of this group. in AOA in paddy field soils after was applied as nitrogen fertilizer. AMMONIA OR AMMONIUM AS SUBSTRATE FOR AMMONIA In some studies, high ammonia appears to promote AOA MONOOXYGENASE growth and activity. Treusch et al. (2005) found considerably + Is ammonia (NH3) or the cation ammonium (NH4 ) the sub- higher amounts of archaeal amoA transcripts in those samples strate for the archaeal AMO enzyme? Ammonia is known to be that had been amended with additional ammonia (10 mM). the substrate of this initial step in bacterial ammonia oxidation It was demonstrated that the soil archaea Nitrososphaera vien- (Suzuki et al., 1974; Arp et al., 2002). However, despite several nensis strain EN76 grows well in media containing ammonium studies dedicated to studying the biochemistry of AMO in bacteria, concentrations as high as 15 mM, but its growth is inhibited it still remains unknown whether ammonia or ammonium is the at 20 mM (Tourna et al., 2011). This is considerably higher substrate for archaeal AMO (Martens-Habbena and Stahl, 2011). than the inhibitory concentration of 2–3 mM reported for the − Bacterial oxidation of ammonia to nitrite (NO2 ) is a two-step aquatic AOA Nitrosopumilus maritimus (Walker et al., 2010) and process. AMO oxidizes ammonia to hydroxylamine (NH2OH), Ca. (Hatzenpichler et al., 2008). Toler- and hydroxylamine oxidoreductase (HAO) catalyzes oxidation of ance for ammonia toxicity of Ca. Nitrosoarchaeum koreensis strain hydroxylamine to nitrite (Arp et al., 2002). Structural differences MY1, isolated from an acidic agricultural soil, was slightly lower, in the archaeal AMO and bacterial AMO and the absence of 5 mM, than that of Nitrososphaera viennensis (Jung et al., 2011). genes encoding HAO and cytochrome c for recycling elec- Park et al. (2006) found archaeal amoA in wastewater with 2 mM trons suggest important differences between bacterial and archaeal ammonia. ammonia oxidation. For example, nitroxyl (HNO) rather than The source of substrate and its location can influence ammonia hydroxylamine may be the intermediate in the AMO enzymatic concentration in soil (Offre et al., 2009; Stopnisek et al., 2010; Ver- reaction, or a different cytochrome system may be responsible for hamme et al., 2011). Ammonium production via mineralization, electron channeling in AOA (Walker et al., 2010). additions of ammonical fertilizers, animal wastes, and the atmo- The majority of AOA discovered to date were found in olig- spheric deposition of ammonium increases substrate supply, while otrophic conditions (Hatzenpichler et al., 2008; Walker et al., competing consumptive processes include microbial assimilation 2010). The affinity of marine archaeon Nitrosopumilus maritimus (immobilization), plant assimilation, and ammonia volatiliza- for ammonium/ammonia was 200-fold higher than substrate tion reduce ammonia concentration (Norton and Stark, 2011).

www.frontiersin.org June 2012 | Volume 3 | Article 210 | 3

“fmicb-03-00210” — 2012/6/13 — 21:04 — page3—#3 Zhalnina et al. Drivers of AOA in soils

In addition, AOA do not respond to the addition of mineral gradient from 4.5 to 7.5 showed a greater proportion of this nitrogentosoil(Di et al., 2009; Jia and Conrad, 2009; Stopnisek group in the most acidic soils (Lehtovirta et al., 2009). Yao et al. et al., 2010; Verhamme et al., 2011; Ke and Lu, 2012). In contrast, (2011) studied nitrification in tea orchard soils with low pH (3.6– AOB increase in abundance after addition of ammonium sulfate 6.3) and found that the high level of nitrification was driven by or urine (Di et al., 2009, 2010; Jia and Conrad, 2009; Hofferle AOA but not AOB. In addition, AOA phylotypes found in highly et al., 2010). Archaeal amoA gene copies and nitrate concentra- acidic soils (pH < 4) were negatively correlated with pH, and tion increased during incubation soil for 30 days (Offre et al., AOA from soils with a higher pH (>4) showed a positive cor- 2009). All ammonia in this soil was generated by nitrogen min- relation with pH (Yao et al., 2011). Zhang et al. (2011) found eralization since no ammonia was added. Also, it was shown archaea in five strongly acidic soils (between pH 4.2 and 4.47) in upland field soils archaeal 16S rRNA gene was significantly where archaeal amoA gene abundance was strongly correlated affected by the class of fertilizer (chemical or organic fertilizer). In with nitrate concentration. Recently Ca. Nitrosotalea devanaterra, four different soil types 16S rRNA abundance of AOA was about the first obligate acidophilic ammonia oxidizer, was discovered 0.1–0.9 × 108 gene copy number higher in the plots where organic and cultured from an agricultural acidic soil (pH 4.5; Lehtovirta- fertilizers were added than in the plots with chemical fertilizer Morley et al., 2011).Thisarchaeonisabletogrowatextremely addition. low concentrations of ammonia (0.18 nM) suggesting that this Nitrate concentrations likely differ greatly both spatially and organism has evolved to tolerate the acidic conditions that make temporally under these two scenarios (Stopnisek et al., 2010). ammonia concentrations very low. As AOB have a lower affinity While ammonia from organic matter mineralization is slowly and for ammonia, the low availability of ammonia under acidic condi- constantly liberated resulting in low, but steady, levels of ammo- tions is believed to be the main reason for decreasing of ammonia nia, an application of mineral nitrogen fertilizer promotes a burst oxidation by AOB in acidic soils (de Boer and Kowalchuk, 2001). of ammonia. Archaeal ammonia oxidizers should be expected to In contrast, the high affinity for ammonia allows certain eco- be in a higher abundance in the soils with high organic matter, types of AOA to grow under low concentrations of ammonia which would provide a constant source of substrate (Stopnisek (Nicol et al., 2008; Martens-Habbena et al., 2009; Gubry-Rangin et al., 2010). et al., 2010). Adaptation to different concentrations of ammonia and the Ammonia-oxidizing archaea also appear dominant under alka- ability to survive even at extremely low concentrations of ammo- line conditions as well as acidic conditions and are often more nia, together with other ecological factors, contribute to the abundant than AOB at higher pH (Shen et al., 2008; Zhang et al., ecological fitness and niche adaptation of AOA and AOB. The 2010; Bates et al., 2011). Shen et al. (2008) did not observe a sig- presence of different ecophysiological adaptations such as different nificant correlation between AOA and pH in the alkaline soils concentrations of substrate suggests that a wide range of ecotypes (pH 8.3–8.7), but the number of archaeal amoA genes did not can be expected to occur among soil AOA. decline with increasing pH. In Cambisol soils (pH 6–6.5), AOA were positively correlated with pH (Wessén et al., 2010). DIFFERENT LINEAGES OF AOA RESIDE AT DIFFERENT pH LEVELS Nitrification in alkaline soils (pH 7.5) by AOA was demon- + Ammonia (NH3), not ammonium (NH4 ), is the likely substrate strated by Zhang et al. (2010). After incubation of soil with carbon for the AMO that catalyzes the initial step of the oxidation of dioxide, archaeal but not bacterial DNA was detected, and the ammonia (Arp et al., 2002). The ammonia form is pH dependent number of archaeal amoA outnumbered bacterial amoA. Bates (pKa = 9.25, 25◦C) and conversions between ionic and cationic et al. (2011) studied changes in bacterial and archaeal communi- forms may occur close to or at the cell membrane (Norton and ties in 146 soils across the globe and found a positive correlation Stark, 2011). between AOA with soil pH, especially in forests and shrub lands. Ammonia-oxidizing archaea are more tolerant to low pH than Bru et al. (2011) investigated the distribution of AOA communi- AOB, and AOA are mainly responsible for nitrification in acidic ties over 107 sites in Burgundy, France, with pH ranging from soils (Leininger et al., 2006; Gubry-Rangin et al., 2010; Yao et al., 4.2 to 8.3 and found that in acidic soils AOA were below the 2011; Zhang et al., 2011; Isobe et al., 2012). Archaeal amoA was detection level and AOA abundance positively correlated with found in conditions as low as pH 2.5 in terrestrial hot springs soil pH. (Reigstad et al., 2008), as high as pH 8.2 in North Sea water Different AOA ecotypes have evolved to growth at different and sediments (Wuchter et al., 2006; Blainey et al., 2011), and pH levels. The existence of different environmental lineages was at pH 9 at Eagleville spring in California (Zhang et al., 2008), suggested by Nicol et al. (2008) and supported by Gubry-Rangin where they were the only representatives of ammonia oxidizers. et al. (2011). Gubry-Rangin et al. (2011) clustered archaeal amoA The lowest pH levels of soil in which AOA have been found are sequences from globally distributed soils that varied widely in 3.6–4.0 (He et al., 2007; Yao et al., 2011). Nicol et al. (2008) pH. They found that all studied phylogenetic lineages were classi- reported that archaeal amoA gene and transcript abundance fied as acidophilic (lineage C – including Group 1.1a-associated), decreased with higher pH during a soil microcosm experiment. acido-neutrophilic (linage A – including Group 1.1a), and alka- Further study revealed an increase in archaeal amoA gene and tran- linophilic (linage B – including Group 1.1b). These lineages vary script abundance during nitrification and inhibition of archaeal in their response to pH but overall, archaeal amoA abundance amoA, but not bacterial amoA, by acetylene addition in two agri- increased with increasing pH. pH appears to be a strong fac- cultural acidic soils (Gubry-Rangin et al., 2010). Quantification tor in many studies, but AOA are successful across a range of of 1.1c crenarchaeal 16S rRNA gene abundance through a pH pH values.

Frontiers in Microbiology | Terrestrial Microbiology June 2012 | Volume 3 | Article 210 | 4

“fmicb-03-00210” — 2012/6/13 — 21:04 — page4—#4 Zhalnina et al. Drivers of AOA in soils

CARBON TEMPERATURE Are AOA autotrophic, heterotrophic, or mixotrophic with Temperature is one of the most significant factors that affect soil regard to carbon utilization? Components of the modified organic matter decomposition, nitrification, and greenhouse gas 3-hydroxypropionate/4-hydroxybutyrate cycle of autotrophic car- production in terrestrial environments (Kirschbaum, 1995; Stark bon assimilation were identified in genomes of Cenarchaeum sym- and Firestone, 1996). Although optimal temperatures for potential biosum (Hallam et al., 2006), Nitrosopumilus maritimus (Walker nitrification are usually between 20 and 37◦C, the AOA produce et al., 2010), Ca. Nitrosotalea devanaterra (Lehtovirta-Morley nitrite at temperatures that vary from −1◦C inArctic coastal waters et al., 2011), and Ca. Nitrosoarchaeum limnia (Blainey et al., to 97◦C in hot springs of Iceland (Reigstad et al., 2008; Kalanetra 2011). Ca. Nitrososphaera gargensis (Hatzenpichler et al., 2008) et al., 2009). and Nitrososphaera viennensis can use carbon dioxide as sole car- Archaeal amoA was detected in near-freezingArctic andAntarc- bon source (Tourna et al., 2011). Zhang et al. (2010) provided tic waters with 4.92 × 106 and 0.18 × 106 copies, respectively direct evidences for autotrophic activity and autotrophic growth (Kalanetra et al., 2009). Christman et al. (2011) analyzed distribu- of Thaumarchaeota in soil. Nitrification rates in this study cor- tion of AOA during summer (T = 5.1◦C) and winter (T =−1.7◦C) related with increased archaeal, but not bacterial, amoA and hcd in the Coastal Arctic Ocean and found that AOA amoA levels and (key gene in 3-hydroxypropionate/4-hydroxybutyrate cycle) genes’ nitrification rates were higher in winter. abundances. Also, stable isotope probing showed incorporation The majority of AOA identified in soil and marine environ- of 13C-labeled carbon dioxide into archaeal amoA during nitri- ments are non-thermophilic and are typically found at tem- fication but not into bacterial amoA. In addition, mRNA-SIP peraturesfrom22to37◦C(Könneke et al., 2005; Hallam et al., supported autotrophic carbon dioxide fixation by AOA using the 2006; Muller et al., 2010; Blainey et al., 2011; Jung et al., 2011; 3-hydroxypropionate/4-hydroxybutyrate cycle in an agricultural Kim et al., 2011; Lehtovirta-Morley et al., 2011; Tourna et al., soil (Pratscher et al., 2011). 2011). The thermophilic AOA detected in deep-sea hydrother- Later evidence builds the case that some AOA take up organic mal vents and hot springs perform nitrification at temperatures carbon compounds, but others may be inhibited by organics. The of 45–97◦C(de la Torre et al., 2008; Hatzenpichler et al., 2008; first finding of the uptake of amino acids by planktonic archaea Reigstad et al., 2008; Wang et al., 2009; Zhang et al., 2011). was shown by Ouverney and Fuhrman (2000). Herndl et al. (2005) A moderately thermophilic (46◦C) archaeon, Ca. Nitrososphaera and Teira et al. (2004) indicated the uptake of amino acids by gargensis, discovered in microbial mats of the Siberian Garga hot isotopic studies of microbial communities in the Atlantic Ocean spring was the dominant ammonia oxidizer in terrestrial non- and speculated that this could be an indication of the utilization thermophilic environments. Archaeal adaptations to function of the dissolved organic matter as an energy source. under elevated temperatures was demonstrated when different Recent sequencing of AOA genomes and the culturing of AOA temperatures for fermenting cattle manure compost revealed have supported mixotrophy by these organisms. Oxidative and growthofAOBat37◦C,whereasAOAcontinuetogrowupto60◦C reductive tricarboxylic acid cycle (TCA) genes were found in (Oishi et al., 2011). the genome Cenarchaeum symbiosum (Hallam et al., 2006). In The impact of different temperatures on AOA populations addition to the genes that code for the 3-hydroxypropionate/ was examined in field and microcosm experiments. Tourna et al. 4-hydroxybutyrate pathway, the Nitrosopumilus maritimus (2008) studied the responses of AOA and AOB during incuba- genome contains genes encoding for the complete oxidative TCA tion of soil microcosms at temperatures in the range 10–30◦C. cycle (Walker et al., 2010) as well as transporters for amino They determined that the most profound changes in patterns of acids, dipeptides/oligopeptides, sulfonates/taurine, and glycerol. archaeal amoA gene transcript abundance occurred at 30◦C. Stres Putative organic carbon consumption was suggested based on et al. (2008) found that soil archaeal, but not bacterial, commu- genome sequence of Ca. Nitrosoarchaeum limnia (Blainey et al., nity structure changed during incubation at higher temperatures. 2011). Increased growth of Nitrososphaera viennensis cultures by A global survey of different soils showed a positive correlation small additions of pyruvate (Tourna et al., 2011) also supports between relative archaeal abundance and annual temperatures, mixotrophic growth by AOA. and temperature became even more significant factor for the Chen et al. (2008) reported a higher abundance of AOA in the relative abundance of archaea from forests and shrub lands (Bates paddy rhizosphere compared to non-rhizosphere soil, presumably et al., 2011). due to organic carbon of root exudates. Increased abundance of 1.1b AOA clade occurred upon the addition of root extract as MOISTURE an organic amendment to the AOA enrichment culture (Xu et al., Soil moisture and temperature impacts on main processes of nitro- 2012). Nevertheless, organic substrates have been shown to inhibit gen cycle, such as organic matter mineralization, nitric and nitrous AOA or be negatively correlated with AOA abundance (Könneke oxide production, nitrogen fixing, and particularly, nitrification et al., 2005; Wessén et al., 2010; Bates et al., 2011). Pester et al. (Kirschbaum, 1995; Zheng et al., 2000; Belnap, 2001; Norton and (2012) also revealed negative correlation of AOA species rich- Stark, 2011). Soil moisture promoted changes in the archaeal com- ness to the organic carbon content in four geographically and munity in grassland soil microcosm (Stres et al., 2008). Bates et al. chemically distinct soils. Although, genetic capacity to potentially (2011) observed a negative correlation of soil moisture in tall grass use organic carbon and some cases of small organic molecules prairies with AOA abundance. Diversity of soil microbial commu- uptake by AOA were found by recent studies, there is still lack of nities along a steep precipitation gradient ranging from an arid understanding how exactly AOA use organic carbon. area with less than 100 mm annual rain to a meso-Mediterranean

www.frontiersin.org June 2012 | Volume 3 | Article 210 | 5

“fmicb-03-00210” — 2012/6/13 — 21:04 — page5—#5 Zhalnina et al. Drivers of AOA in soils

forest receiving over 900 mm precipitation was studied. Of mea- copies per gram dry soil). Moreover, AOA reacted faster to the sured physicochemical factors, water content was found to have the presence of oxygen in fluctuating oxic and anoxic rhizosphere strongest correlation with the bacterial and archaeal community of rice plants compared to AOB (Chen et al., 2008). Enrichment structures in studied soils (Angel et al., 2010). culture of Ca. Nitrososphaera gargensis was grown aerobically at Study of nitrogen and water amendment in two temperate DO concentrations 0.15–1.18 mM. Kinetic respirometry assays forest soils revealed that the AOA community composition was showed that Ca. Nitrosoarchaeum koreensis strain MY1’s affini- sensitive to moisture content in one of the soils and archaeal ties for oxygen (1.08 μM) were much higher than those of AOB amoA genes were more abundant at 40% than 70% water-filled (Jung et al., 2011). pore space suggesting reduced oxygen levels lowered AOA growth Among the factors listed above there are many other factors (Szukics et al., 2012). that were shown to have some impact on AOA community. These include altitude (Zhang et al., 2009), soil types (Hoshino et al., OXYGEN AND OTHER FACTORS 2011; Morimoto et al., 2011), sulfide (Caffrey et al., 2007; Coolen Oxygen plays an important role in nitrification as a substrate for et al., 2007), phosphate (Herfort et al., 2007), and salinity (Bern- the AMO enzyme and as terminal electron acceptor (Arp et al., hard et al., 2010). However, these factors either do not have a 2002). In soil, oxygen levels are balanced by oxygen consumption significant impact on archaeal ammonia oxidation or have not and diffusion from the surface through the air-filled pores (Sex- been found to influence soil AOA. stone et al., 1985). Nitrification usually declines in soil if water levels have exceeded field capacity for several days (Schjonning CONCLUDING REMARKS et al., 2003) thereby decreasing oxygen content. Tolerance to low The AOA are a versatile, ubiquitous, and abundant group of concentrations of DO was demonstrated in activated sludge biore- microorganisms that have adapted to survive in a wide variety actors with low DO (<6.3 μM; Park et al., 2006). In subterranean of harsh environments. Moreover, their important function in estuaries at low-oxygen fresh and brackish stations, AOA were the nitrogen cycle, and their roles in nitrate leaching, green- 10 times more abundant than AOB (Santoro et al., 2011). Bouskill house gas production, and soil subsidence make the AOA a et al. (2012) examined the distribution AOA across large-scale gra- group that deserves further studies. Knowing the main drivers dients in DO as one of the important factors of AOA distribution of AOA abundance and distribution in soil is of growing inter- in marine environments. The highest abundance of the AOA amoA est around the world. There are many studies that assess marine gene was recorded in the oxygen minimum zones (OMZs) of the environmental AOA communities, but much less is known about Eastern Tropical South Pacific (ETSP) and the Arabian Sea (AS). soil AOA. Soil features that have major influence on shaping AOA in the AS exhibited a very narrow range of preferred oxy- AOA communities include ammonia concentration, pH, organic gen conditions (5–2.5 μM; Pitcher et al., 2011). Stoichiometry matter, moisture, temperature, and oxygen. AOA possess high and kinetic of ammonium oxidation by Nitrosopumilus maritimus affinities for ammonia and oxygen and can tolerate extremes showed the endogenous oxygen uptake of the cells was consis- of temperature and pH. These features explain why the AOA tently below 0.5 μM per hour, but after addition of ammonium greatly outnumber the AOB in many soils and other environ- to the cells, oxygen uptake increased within a few minutes up to ments, as they can inhabit potential niches that are not available to − 30 μMh 1 and remained high until the ammonium level declined the AOB. below 1 μM(Martens-Habbena and Stahl, 2011). AOA and AOB are adapted to life in low-oxygen or periodically anoxic habitats in ACKNOWLEDGMENT paddy soils. Although flooding paddy soil is predominantly anaer- Publication of this article was funded in part by the University of obic, large numbers of AOA were detected (8.31 × 107–2.12 × 108 Florida Open-Access Publishing Fund.

REFERENCES in biological soil crusts,” in Biolog- 1–12. doi: 10.1371/journal.pone. communities at the landscape scale. Angel, R., Soares, M. I., Ungar, E. D., ical Soil Crusts: Structure, Function, 0016626 ISME J. 5, 532–542. and Gillor, O. (2010). Biogeography and Management. Ecological Studies, Bouskill, N. J., Eveillard, D., Chien, Caffrey, J. M., Bano, N., Kalan- of soil archaea and bacteria along a Vol. 150, eds J. Belnap and O. D., Jayakumar, A., and Ward, etra, K., and Hollibaugh, J. steep precipitation gradient. ISME J. L. Lange (Springer Verlag: Berlin), B. B. (2012). Environmental fac- T. (2007). Ammonia oxidation 4, 553–563. 241–261. tors determining ammonia-oxidizing and ammonia-oxidizing bacteria and Arp, D. J., Sayavedra-Soto, L. A., and Bernhard, A. E., Landry, Z. C., Blevins, organism distribution and diversity archaea from estuaries with differ- Hommes, N. G. (2002). Molec- A., de la Torre, J. R., Giblin, A. in marine environments. Environ. ing histories of hypoxia. ISME J. 1, ular biology and biochemistry of E., and Stahl, D. A. (2010). Abun- Microbiol. 14, 714–729. 660–662. ammonia oxidation by Nitrosomonas dance of ammonia-oxidizing archaea Brochier-Armanet, C., Boussau, B., Chen, X., Zhu, Y., Xia, Y., Shen, J., and europaea. Arch. Microbiol. 178, and bacteria along an estuarine salin- Gribaldo, S., and Forterre, P. (2008). He, J. (2008). Ammonia-oxidizing 250–255. ity gradient in relation to poten- Mesophilic crenarchaeota: proposal archaea: important players in paddy Bates, S. T., Berg-Lyons, D., Capo- tial nitrification rates. Appl. Environ. for a third archaeal phylum, the rhizosphere soil? Environ. Microbiol. raso, J. G., Walters, W. A., Knight, Microbiol. 76, 1285–1289. Thaumarchaeota. Nat. Rev. Micro- 10, 1978–1987. R., and Fierer, N. (2011). Examining Blainey, P. C., Mosier, A. C., Potan- biol. 6, 245–252. Christman, G. D., Cottrell, M. T., the global distribution of dominant ina, A., Francis, C. A., and Quake, S. Bru, D., Ramette, A., Saby, N. P. Popp, B. N., Gier, E., and Kirch- archaeal populations in soil. ISME J. R. (2011). Genome of a low-salinity A., Dequiedt, S., Ranjard, L, Jolivet, man, D. L. (2011). Abundance, 5, 908–917. ammonia-oxidizing archaeon deter- C., Arrouays D., and Philippot, L. diversity, and activity of ammonia- Belnap, J. (2001). “Factors influencing mined by single-cell and metage- (2011). Determinants of the distri- oxidizing prokaryotes in the coastal nitrogen fixation and nitrogen release nomic analysis. PLoS ONE 6, bution of nitrogen-cycling microbial arctic ocean in summer and winter.

Frontiers in Microbiology | Terrestrial Microbiology June 2012 | Volume 3 | Article 210 | 6

“fmicb-03-00210” — 2012/6/13 — 21:04 — page6—#6 Zhalnina et al. Drivers of AOA in soils

Appl. Environ. Microbiol. 77, 2026– Richardson, P. M., and DeLong, deposition. FEMS Microbiol. Ecol. 80, Martens-Habbena, W., Berube, P. 2034. E. F. (2006). Pathways of car- 193–203. M, Urakawa, H., de la Torre, Colliver, B. B., and Stephenson, T. bon assimilation and ammonia oxi- Jia, Z. J., and Conrad, R. (2009). Bac- J. R, and Stahl, D. A. (2009). (2000). Production of nitrogen oxide dation suggested by environmental teria rather than Archaea dominate Ammonia oxidation kinetics deter- and dinitrogen oxide by autotrophic genomic analyses of marine Crenar- microbial ammonia oxidation in an mines niche separation of nitrifying nitrifiers. Biotechnol. Adv. 18, chaeota. PLoS Biol. 4, 0520–0536. doi: agricultural soil. Environ. Microbiol. Archaea and Bacteria. Nature 461, 219–232. 10.1371/journal.pbio.0040095 11, 1658–1671. 976–979. Coolen, M. J. L., Abbas, B., van Blei- Hastings, R. S., Butler, C., Singleton, Jung, M. Y., Park, S. J., Min, D., Kim, J. Martens-Habbena, W., and Stahl, D. jswijk, J., Hopmans, E. C., Kuypers, I., Saunders, J. R., and McCarthy, S., Rijpstra, W. I., Damsté, J. S., Kim, A. (2011). Nitrogen metabolism M. M. M., Wakeham, S. G., and Sin- A. J. (2000). Analysis of ammonia- G. J., Madsen, E. L., and Rhee, S. K. and kinetics of ammonia-oxidizing ninghe Damste, J. S. (2007). Putative oxidizing bacteria populations in acid (2011). Enrichment and characteri- archaea. Methods Enzymol. 496, ammonia-oxidizing crenarchaeota in forest soil during conditions of mois- zation of an autotrophic ammonia- 465–487. suboxic waters of the Black Sea: a ture limitation. Lett. Appl. Microbiol. oxidizing archaeon of mesophilic Morimoto, S., Hayatsu, M., Hoshino, basin-wide ecological study using 16S 30, 14–18. crenarchaeal Group I.1a from an agri- Y. T., Nagaoka, K., Yamazaki, M., ribosomal and functional genes and Hatzenpichler, R., Lebedeva, E. V., cultural soil. Appl. Environ. Micro- Karasawa, T., Takenaka, M., and membrane lipids. Environ. Microbiol. Spieck, E., Stoecker, K., Richter, A., biol. 77, 8635–8647. Akiyama, H. (2011). Quantitative 9, 1001–1016. Daims, H., and Wagner, M. (2008). A Kalanetra, K. M., Bano, N., and Hol- analyses of ammonia-oxidizing arc- de Boer, W., and Kowalchuk, G. A. moderately thermophilic ammonia- libaugh, J. T. (2009). Ammonia- haea (AOA) and ammonia-oxidizing (2001). Nitrification in acid soils: oxidizing crenarchaeote from a hot oxidizing Archaea in the Arctic Ocean bacteria (AOB) in fields with differ- microorganisms and mechanisms. spring. Proc. Natl. Acad. Sci. U.S.A. and Antarctic coastal waters. Environ. ent soil types. Microbes Environ. 26, Soil Biol. Biochem. 33, 853–866. 6, 2134–2139. Microbiol. 11, 2434–2445. 248–253. de la Torre, J. R., Walker, C. B., Ingalls, He, J., Shen, J., Zhang, L., Zhu, Y., Ke, X., and Lu, Y. (2012). Adapta- Muller, F., Brissac, T., Le Bris, N., Fel- A. E., Könneke, M., and Stahl, D. A. Zheng, Y., Xu, M., and Di, H. tion of ammonia-oxidizing microbes beck H., and Gros, O. (2010). First (2008). Cultivation of a thermophilic (2007). Quantitative analyses of to environment shift of paddy field description of giant Archaea (Thau- ammonia oxidizing archaeon synthe- the abundance and composition soil. FEMS Microbiol. Ecol. 80, marchaeota) associated with putative sizing . Environ. Micro- of ammonia-oxidizing bacteria and 87–97. bacterial ectosymbionts in a sulfidic biol. 10, 810–818. ammonia-oxidizing archaea of a Chi- Kim, B. K., Jung, M. Y., Yu, D. S., marine habitat. Environ. Microbiol. Di, H. J., Cameron, K. C., Shen, J. nese upland red soil under long- Park, S. J., Oh, T. K., Rhee, S. 12, 2371–2383. P., Winefield, C. S., O’Callaghan, term fertilization practices. Environ. K., and Kim, J. F. (2011). Genome Nicol, G. W., Leininger, S., Schleper, M., Bowatte, S., and He, J. Z. Microbiol. 9, 2364–2374. sequence of an ammonia-oxidizing C., and Prosser, J. I. (2008). The (2009). Nitrification driven by bac- Herfort, L., Schouten, S., and Abbas, B. soil archaeon,“Candidatus Nitrosoar- influence of soil pH on the diversity, teria and not archaea in nitrogen- (2007). Variations in spatial and tem- chaeum koreensis” MY1. J. Bacteriol. abundance and transcriptional activ- rich grassland soils. Nat. Geosci. 2, poral distribution of Archaea in the 193, 5539–5540. ity of ammonia oxidizing archaea 621–624. North Sea in relation to environmen- Kirschbaum, M. U. (1995). The tem- and bacteria. Environ. Microbiol. 10, Di, H. J., Cameron, K. C., Shen, J. tal variables. FEMS Microbiol. Ecol. perature dependence of soil organic 2966–2978. P., Winefield, C. S., O’Callaghan, 62, 242–257. matter decomposition, and the effect Norton, J. M., and Stark, J. M. M., Bowatte, S., and He, J. Z. Hermansson, A., and Lindgren, P. E. of global warming on soil organic (2011). Regulation and measure- (2010). Ammonia-oxidizing bacteria (2001). Quantification of ammonia- Cstorage. Soil Biol. Biochem. 27, ment of nitrification in terrestrial and archaea grow under contrast- oxidizing bacteria in arable soil by 753–760. systems. Methods Enzymol. 486, ing soil nitrogen conditions. FEMS real-time PCR. Appl. Environ. Micro- Könneke, M., Bernhard, A. E., de la 343–368. Microbiol. Ecol. 72, 386–394. biol. 67, 972–976. Torre, J. R., Walker, C. B., Waterbury, Offre, P., Prosser, J. I., and Nicol, Erguder, T. H., Boon, N., Wittebolle, Herndl, G. J., Reinthaler, T., Teira, E., J. B., and Stahl, D. A. (2005). Iso- G. W. (2009). Growth of ammonia- L., Marzorati, M., and Verstraete, Aken, H., Veth, C., Pernthaler, A., lation of an autotrophic ammonia- oxidizing archaea in soil microcosms W. (2009). Environmental factors and Pernthaler, J. (2005). Contri- oxidizing marine archaeon. Nature is inhibited by acetylene. FEMS shaping the ecological niches of bution of Archaea to total prokary- 437, 543–546. Microbiol. Ecol. 70, 99–108. ammonia-oxidizing archaea. FEMS otic production in the deep Atlantic Kowalchuk, G. A., and Stephen, J. A. Oishi, R., Tada, C., Asano, R., Yama- Microbiol. Ecol. Rev. 33, 855–869. ocean. Appl. Environ. Microbiol. 71, (2001). Ammonia-oxidizing bacte- moto, N., Suyama, Y., and Nakai, Ghosh, P., and Dhyani, P. P. (2005). 2303–2309. ria: a model for molecular microbial Y. (2011). Growth of ammonia- Nitrogen mineralization, nitrifica- Hofferle, S., Nicol, G. W., Pal, L., ecology. Annu.Rev.Microbiol.55, oxidizing archaea and bacteria in cat- tion and nitrifier population in Hacin, J., Prosser, J. I., and Mandic- 485–529. tle manure compost under various a protected grassland and rainfed Mulec, I. (2010). Ammonium supply Lehtovirta, L. E., Prosser, J. E., and temperatures and ammonia concen- agricultural soil. Trop. Ecol. 46, rate influences archaeal and bacterial Nicol, G. W. (2009). Soil pH regulates trations. Microbes Ecol. doi: 10.1007/ 173–181. ammonia oxidizers in a wetland soil the abundance and diversity of Group s00248-011-9971-z [Epub ahead of Gubry-Rangin, C., Hai, B., Quince, C., vertical profile. FEMS Microbiol. Ecol. 1.1c Crenarchaeota. FEMS Microbiol. print]. Engel, M., Thomson, B. C., James, 74, 302–315. Ecol. 70, 367–376. Oldeman, L. R., Hakkeling, R. T. A., and P., Schloter, M., Griffiths, R. I., Hoshino, Y. T., Morimoto, S., Hayatsu, Lehtovirta-Morley, L. E., Stoecker, K., Sombroek, W. G. (1991). World Map Prosser, J. I., and Nicol, G. W. (2011). M., Nagaoka, K., Suzuki, C., Kara- Vilcinskas, A., Prosser, J. I., and Nicol, of the Status of Human-induced Soil Niche specialization of terrestrial sawa, T., Takenaka, M., and Akiyama, G. W. (2011). Cultivation of an obli- Degradation (GLASOD): An Explana- archaeal ammonia oxidizers. Proc. H. (2011). Effect of soil type and fer- gate acidophilic ammonia oxidizer tory Note. Wageningen: Interna- Natl. Acad. Sci. U.S.A. 108, 21206– tilizer management on archaeal com- from a nitrifying acid soil. Proc. Natl. tional Soil Reference and Information 21211. munity in upland field soils. Microbes Acad. Sci. U.S.A. 108, 15892–15897. Centre. Gubry-Rangin, C., Nicol, G. W., and Environ. 26, 307–316. Leininger, S., Urich, T., Schloter, Ouverney, C. C., and Fuhrman, J. A. Prosser, J. I. (2010). Archaea rather Isobe, K., Koba, K., Suwa, Y., Ikutani, M., Schwark, L., Qi, J., Nicol, G. (2000). Marine planktonic archaea than bacteria control nitrification in J., Fang, Y., Yoh, M., Mo, J., Otsuka, W., Prosser, J. I., Schuster, S. C., and take up amino acids. Appl. Environ. two agricultural acidic soils. FEMS S., and Senoo, K. (2012). High abun- Schleper, C. (2006). Archaea predom- Microbiol. 66, 4829–4833. Microbiol. Ecol. 74, 566–574. dance of ammonia-oxidizing archaea inate among ammonia-oxidizing Park, H.,Wells, G. F., Bae, H., Criddle, C. Hallam, S. J., Mincer, T. J., Schleper, in acidified subtropical forest soils prokaryotes in soils. Nature 442, S., and Francis, C. A. (2006). Occur- C., Preston, C. M., Roberts, K., in southern China after long-term N 806–809. rence of ammonia-oxidizing archaea

www.frontiersin.org June 2012 | Volume 3 | Article 210 | 7

“fmicb-03-00210” — 2012/6/13 — 21:04 — page7—#7 Zhalnina et al. Drivers of AOA in soils

in wastewater treatment plant biore- Schjonning, P., Thomsen, I. K., Mol- A. (2012). Rapid and dissimi- N., Arp, D. J., Brochier-Armanet, actors. Appl. Environ. Microbiol. 72, drup, P., and Christensen, B. T. lar response of ammonia oxidizing C., Chain, P. S., Chan, P. P., Gol- 5643–5647. (2003). Linking soil microbial activ- archaea and bacteria to nitrogen and labgir, A., Hemp, J., Hügler, M., Pelve, E., Lindås, A. C., Martens- ity to water- and air-phase contents water amendment in two temper- Karr, E. A., Könneke, M., Shin, M., Habbena, W., de la Torre, J. R., Stahl, and diffusivities. Soil Sci. Soc. Am. J. ate forest soils. Microbiol. Res. 67, Lawton, T. J., Lowe, T., Martens- D. A., and Bernander, R. (2011). 67, 156–165. 103–109. Habbena, W., Sayavedra-Soto, L. A., Cdv-based cell division and cell Schleper, C. (2010). Ammonia oxida- Teira, E., Reinthaler, T., Pernthaler, Lang, D., Sievert, S. M., Rosenzweig, cycle organization in the thaumar- tion: different niches for bacteria and A., Pernthaler, J., and Herndl, A. C., Manning, G., and Stahl, D. chaeon Nitrosopumilus maritimus. archaea? ISME J. 4, 1092–1094. G. J. (2004). Combining catalyzed A. (2010). Nitrosopumilus maritimus Mol. Microbiol. 82, 555–566. Sexstone, A. J., Revsbech, N. P., Parkin, reporter deposition-fluorescence in genome reveals unique mechanisms Pester, M., Rattei, T., Flench, S., T. B., and Tiedje, J. M. (1985). situ hybridization and microautora- for nitrification and autotrophy in Gröngröft, A., Richter, A., Over- Direct measurement of oxygen pro- diography to detect substrate utiliza- globally distributed marine crenar- mann, J., Reinhold-Hurek, B., files and denitrification rates in soil tion by bacteria and archaea in the chaea. Proc. Natl. Acad. Sci. U.S.A. Loy, A., and Wagner, M. (2012). aggregates. Soil Sci. Soc. Am. J. 49, deep ocean. Appl. Environ. Microbiol. 107, 8818–8823. amoA-based consensus phylogeny 645–651. 70, 4411–4414. Wang, S., Xiao, X., Jiang, L., Peng, of ammonia-oxidizing archaea and Shaw, L. J., Nicol, G. W., Smith, Z., Tourna, M., Freitag, T. E., Nicol, G. X., Zhou, H., Meng, J., and Wang, deep sequencing of amoA genes from Fear, J., Prosser, J. I., and Baggs, E. M. W., and Prosser, J. I. (2008). Growth, F. (2009). Diversity and abundance soils of four different geographic (2006). Nitrosospira spp. can produce activity and temperature responses of ammonia-oxidizing archaea in regions. Environ. Microbiol. 14, nitrous oxide via a nitrifier denitrifi- of ammonia-oxidizing archaea and hydrothermal vent chimneys of the 525–539. cation pathway. Environ. Microbiol. 8, bacteria in soil microcosms. Environ. Juan de Fuca Ridge. Appl. Environ. Pitcher, A., Villanueva, L., Hopmans, E. 214–222. Microbiol. 10, 1357–1364. Microbiol. 75, 4216–4220. C., Schouten, S., Reichart, G., and Shen, J., Zhang, L., Zhu, Y., Zhang, J., Tourna, M., Freitag, T. E., and Prosser, J. Wessén, E., Nyberg, K., Jansson, J. Sinninghe Damste, J. S. (2011). Niche and He, J. (2008). Abundance and I. (2010). Stable isotope probing anal- K., and Hallin, S. (2010). Responses segregation of ammonia-oxidizing composition of ammonia-oxidizing ysis of interactions between ammonia of bacterial and archaeal ammonia archaea and bacteria in the bacteria and ammonia-oxidizing oxidizers. Appl. Environ. Microbiol. oxidizers to soil organic and fertil- Arabian Sea oxygen minimum zone. archaea communities of an alkaline 76, 2468–2477. izer amendments under long-term ISME J. 5, 1896–1904. sandy loam. Environ. Microbiol. 10, Tourna, M., Stieglmeier, M., Spang, management. Appl. Soil Ecol. 45, Pratscher, J., Dumont, M. J., and Con- 1601–1611. A., Könneke, M., Schintlmeister, A., 193–200. rad, R. (2011). Ammonia oxidation Spang, A., Hatzenpichler, R., Brochier- Urich, T., Engel, M., Schloter, M., Wuchter, C., Abbas, B., Coolen, M., coupled to CO2 fixation by archaea Armanet, C., Rattei, T., Tischler, Wagner, M., Richter, A., and Schleper, Herfort, L., Bleijswijk, J., Timmers, and bacteria in an agricultural soil. P., Spieck, E., Streit, W., Stahl, D. C. (2011). Nitrososphaera viennensis, P., Strous, M., Teira, E., Herndl, G. Proc. Natl. Acad. Sci. U.S.A. 108, A., Wagner, M., and Schleper, C. an ammonia oxidizing archaeon from J., Middelburg, J. J., Schouten, S., 4170–4175. (2010). Distinct gene set in two dif- soil. Proc. Natl. Acad. Sci. U.S.A. 20, and Sinninghe Damsté, J. S. (2006). Preston, C. M., Wu, K. M., Molin- ferent lineages of ammonia-oxidizing 8420–8425. Archaeal nitrification in the ocean. ski, T. F., and Delong, E. F. (1996). archaea supports the phylum Thau- Treusch, A. H., Leininger, S., Kletzin, Proc. Natl. Acad. Sci. U.S.A. 103, A psychrophilic crenarchaeon inhab- marchaeota. Trends Microbiol. 18, A., Schuster, S. C., Klenk, H. P., 12317–12322. its a marine sponge: Cenarchaeum 331–340. and Schleper, C. (2005). Novel genes Yao, H., Gao, Y., Nicol, G. W., Camp- symbiosum gen. nov., sp. nov. Stark, J. M., and Firestone, M. for nitrite reductase and Amo-related bell, C. D., Prosser, J. I., Zhang, L., Proc. Natl. Acad. Sci. U.S.A. 93, K. (1996). Kinetic characteristics proteins indicate a role of uncul- Han, W., and Singh, B. K. (2011). 6241–6246. of ammonium-oxidizer communities tivated mesophilic crenarchaeota in Links between ammonia oxidizer Ravishankara, A. R., Daniel, J. in California oak woodland-annual nitrogen cycling. Environ. Microbiol. community structure, abundance, S., and Portmann, R. W. (2011). grassland. Soil Biol. Biochem. 28, 7, 1985–1995. and nitrification potential in acidic Nitrous oxide (N2O): the dominant 1307–1317. van Groenigen, K. J., Osenberg, C. soils. Appl. Environ. Microbiol. 77, ozone-depleting substance emitted Stopnisek, N., Gubry-Rangin, C., Höf- W., and Hungate, B. A. (2011). 4618–4625. in the 21st century. Science 326, ferle, S., Nicol, G. W., Mandic- Increased soil emissions of potent Xu, M., Schnorr, J., Brandon Keibler, 123–125. Mulec, I., and Prosser, J. I. (2010). greenhouse gases under increased B., and Simon, H. M. (2012). Reigstad, L. J., Richter, A., Daims, H., Thaumarchaeal ammonia oxidation atmospheric CO2. Nature 475, Comparative analysis of 16S rRNA Urich, T., Schwark, L., and Schleper, in an acidic forest peat soil is not 214–216. and amoA genes from archaea C. (2008). Nitrification in terrestrial influenced by ammonium amend- Verhamme, D. T., Prosser, J. I., and selected with organic and inor- hot springs of Iceland and Kam- ment. Appl. Environ. Microbiol. 76, Nicol, G. W. (2011). Ammonia ganic amendments in enrichment chatka. FEMS Microbiol. Ecol. 64, 7626–7634. concentration determines differen- culture. Appl. Environ. Microbiol. 78, 167–174. Stres, B., Danevcic, T., Pal, L., Fuka, tial growth of ammonia-oxidizing 2137–2146. Santoro, A. E., Buchwald, C., McIlvin, M. M., Resman, L., Leskovec, S., archaea and bacteria in soil micro- Zhang, C. L., Ye, Q., Huang, Z., Li, W., M. R., and Casciotti, K. L. (2011). Iso- Hacin, J., Stopar, D., Mahne, I., cosms. ISME J. 5, 1067–1071. Chen, J., Song, Z., Zhao, W., Bagwell, topic signature of N2Oproducedby and Mandic-Mulec, I. (2008). Influ- Venter, C. J., Remington, K., Heidel- C., Inskeep, W. P., Ross, C., Gao, L., marine ammonia-oxidizing archaea. ence of temperature and soil water berg, K. J., Halpern, A. L., Rusch, Wiegel, J., Romanek, C. S., Shock, E. Science 333, 1282–1285. content on bacterial, archaeal and D., Eisen, J. A., Wu, D., Paulsen, I., L., and Hedlund, B. P. (2008). Global Schauss, K., Focks, A., Leininger, S., denitrifying microbial communities Nelson, K. E., Nelson, W., Fouts, D. occurrence of archaeal amoA genes in Kotzerke, A., Heuer, H., Thiele- in drained fen grassland soil micro- E., Levy, S., Knap, A. H., Lomas, M. terrestrial hot springs. Appl. Environ. Bruhn, S., Sharma, S., Wilke, cosms. FEMS Microbiol. Ecol. 66, W., Nealson, K., White, O., Peterson, Microbiol. 74, 6417–6426. B. M., Matthies, M., Smalla, K., 110–122. J., Hoffman, J., Parsons, R., Baden- Zhang, L., Hu, H., Shen, J., and Munch, J. C., Amelung, W., Kau- Suzuki, I., Dular, U., and Kwok, S. C. Tillson, H., Pfannkoch, C., Rogers, He, J. (2011). Ammonia-oxidizing penjohann, M., Schloter, M., and (1974). Ammonia or ammonium ion Y. H., and Smith, H. O. (2004). Envi- archaea have more important role Schleper, C. (2009). Dynamics and as substrate for oxidation by Nitro- ronmental genome shotgun sequenc- than ammonia-oxidizing bacteria in functional relevance of ammonia- somonas europaea cells and extracts. ing of the Sargasso Sea. Science 304, ammonia oxidation of strongly acidic oxidizing Archaea in two agricul- J. Bacteriol. 120, 1181–1191. 66–74. soils. ISME J. 6, 1032–1045. tural soils. Environ. Microbiol. 11, Szukics, U., Hackla, E., Zechmeister- Walker, C. B., de la Torre, J. R., Zhang, L., Offre, P. R., He, J. Z., Ver- 446–456. Boltenstern, S., and Sessitsch, Klotz, M. G., Urakawa, H., Pinela, hamme, D. T., Nicol, G. W., and

Frontiers in Microbiology | Terrestrial Microbiology June 2012 | Volume 3 | Article 210 | 8

“fmicb-03-00210” — 2012/6/13 — 21:04 — page8—#8 Zhalnina et al. Drivers of AOA in soils

Prosser, J. I. (2010). Autotrophic L. (2000). Impacts of soil moisture could be construed as a potential con- This article was submitted to Frontiers ammonia oxidation by soil thaumar- on nitrous oxide emission from crop- flict of interest. in Terrestrial Microbiology, a specialty of chaea. Proc. Natl. Acad. Sci. U.S.A. lands: a case study on the rice-based Frontiers in Microbiology. 107, 17240–17245. agro- in Southeast China. Received: 15 March 2012; paper pend- Copyright © 2012 Zhalnina, Dörr de Zhang, L. M., Wang, M., Prosser, J. I., Chemosphere Global Change Sci. 2, ing published: 05 May 2012; accepted: Quadros, Camargo and Triplett. This is Zheng, Y. M., and He, J. Z. (2009). 207–224. 22 May 2012; published online: 15 June an open-access article distributed under Altitude ammonia-oxidizing bacte- 2012. the terms of the Creative Commons ria and archaea in soils of Mount Citation: Zhalnina K, Dörr de Quadros Attribution Non Commercial License, Everest. FEMS Microbiol. Ecol. 70, Conflict of Interest Statement: The P, Camargo FAO and Triplett EW (2012) which permits non-commercial use, dis- 208–217. authors declare that the research was Drivers of archaeal ammonia-oxidizing tribution, and reproduction in other Zheng, X., Wang, M., Wang, Y., Shen, conducted in the absence of any com- communities in soil. Front. Microbio. forums, provided the original authors and R., Ji Gou, J., Li, J., Jin, J., and Li, mercial or financial relationships that 3:210. doi: 10.3389/fmicb.2012.00210 source are credited.

www.frontiersin.org June 2012 | Volume 3 | Article 210 | 9

“fmicb-03-00210” — 2012/6/13 — 21:04 — page9—#9