Abstract
To test if different niches for potential nitrifiers exist in estuarine systems, we assessed by pyrosequencing the diversity of archaeal gene transcript markers for taxonomy (16S ribosomal RNA (rRNA)) during an entire year along a salinity gradient in surface waters of the Charente estuary (Atlantic coast, France). We further investigated the potential for estuarine prokaryotes to oxidize ammonia and hydrolyze urea by quantifying thaumarchaeal amoA and ureC and bacterial amoA transcripts. Our results showed a succession of different nitrifiers from river to sea with bacterial amoA transcripts dominating in the freshwater station while archaeal transcripts were predominant in the marine station. The 16S rRNA sequence analysis revealed that Thaumarchaeota marine group I (MGI) were the most abundant overall but other archaeal groups like Methanosaeta were also potentially active in winter (December–March) and Euryarchaeota marine group II (MGII) were dominant in seawater in summer (April–August). Each station also contained different Thaumarchaeota MGI phylogenetic clusters, and the clusters’ microdiversity was associated to specific environmental conditions suggesting the presence of ecotypes adapted to distinct ecological niches. The amoA and ureC transcript dynamics further indicated that some of the Thaumarchaeota MGI subclusters were involved in ammonia oxidation through the hydrolysis of urea. Our findings show that ammonia-oxidizing Archaea and Bacteria were adapted to contrasted conditions and that the Thaumarchaeota MGI diversity probably corresponds to distinct metabolisms or life strategies.
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References
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689
Auguet JC, Casamayor EO (2008) A hotspot for cold Crenarchaeota in the neuston of high mountain lakes. Environ Microbiol 10:1080–1086
Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K et al (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4:e95
Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP et al (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995
Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74
Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546
Galand PE, Gutierrez-Provecho C, Massana R, Gasol J, Casamayor EO (2010) Inter-annual recurrence of archaeal assemblages in the coastal NW Mediterranean Sea. Limnol Oceanogr 55:2117–2125
Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM et al (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162–1175
Hugoni M, Etien S, Bourges A, Lepere C, Domaizon I et al (2013) Dynamics of ammonia-oxidizing Archaea and Bacteria in contrasted freshwater ecosystems. Res Microbiol 164:360–370
Vissers EW, Anselmetti FS, Bodelier PL, Muyzer G, Schleper C et al (2013) Temporal and spatial coexistence of archaeal and bacterial amoA genes and gene transcripts in Lake Lucerne. Archaea 2013:289478
Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2:429–441
Magalhães C, Machado A, Bordalo A (2009) Temporal variability in the abundance of ammonia oxidizing Bacteria vs. Archaea in sandy sediments of the Douro River estuary, Portugal. Aquat Microb Ecol 56:13–23
Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing Archaea and Bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016
Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing Bacteria and Archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079
Bernhard AE, Bollmann A (2010) Estuarine nitrifiers: new players, patterns and processes. Estuar Coast Shelf Sci 88:1–11
Auguet JC, Triado-Margarit X, Nomokonova N, Camarero L, Casamayor EO (2012) Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake. ISME J 6:1786–1797
Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H et al (2014) Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc Natl Acad Sci U S A 111:12504–12509
Alonso-Saez L, Waller AS, Mende DR, Bakker K, Farnelid H et al (2012) Role for urea in nitrification by polar marine Archaea. Proc Natl Acad Sci U S A 109:17989–17994
Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N et al (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine Crenarchaea. Proc Natl Acad Sci U S A 107:8818–8823
Pedneault E, Galand PE, Potvin M, Tremblay JE, Lovejoy C (2014) Archaeal amoA and ureC genes and their transcriptional activity in the Arctic Ocean. Sci Rep 4:4661
Beam JP, Jay ZJ, Kozubal MA, Inskeep WP (2014) Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park. ISME J 8:938–951
Konneke M, Schubert DM, Brown PC, Hugler M, Standfest S et al (2014) Ammonia-oxidizing Archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc Natl Acad Sci U S A 111:8239–8244
Herlemann DP, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579
Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50:1697–1706
Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440
Auguet JC, Barberan A, Casamayor EO (2009) Global ecological patterns in uncultured Archaea. ISME J 4:182–190
Bernhard AE, Tucker J, Giblin AE, Stahl DA (2007) Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ Microbiol 9:1439–1447
Santoro AE, Casciotti K, Francis CA (2010) Activity, abundance and diversity of nitrifying Archaea and Bacteria in the central California Current. Environ Microbiol Rep 12:1989–2006
Galand PE, Lovejoy C, Pouliot J (2008) Microbial community diversity and heterotrophic production in a coastal Arctic ecosystem: a Stamukhi lake and its source waters. Limnol Oceanogr 53:813–823
Galand PE, Lovejoy C, Vincent WF (2006) Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat Microb Ecol 44:115–126
Herfort L, Kim JH, Coolen MJL, Abbas B, Schouten S et al (2009) Diversity of Archaea and detection of crenarchaeotal amoA genes in the river Rhine and Têt. Aquat Microb Ecol 55:189–201
Alonso-Saez L, Balague V, Sa EL, Sanchez O, Gonzalez JM et al (2007) Seasonality in bacterial diversity in north-west Mediterranean coastal waters: assessment through clone libraries, fingerprinting and FISH. FEMS Microbiol Ecol 60:98–112
Mary I, Cummings DG, Biegala IC, Burkill PH, Archer SD et al (2006) Seasonal dynamics of bacterioplankton community structure at a coastal station in the western English Channel. Aquat Microb Ecol 42:119–126
Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare Bacteria in a coastal ocean. Proc Natl Acad Sci U S A 108:12776–12781
Hugoni M, Taib N, Debroas D, Domaizon I, Jouan Dufournel I et al (2013) Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc Natl Acad Sci U S A 110:6004–6009
Lorenzen CJ (1967) Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346
Strickland J, Parsons T (1968) A practical handbook of sea water analysis
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712
Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072
Kim M, Morrison M, Yu Z (2011) Evaluation of different partial 16S rRNA gene sequence regions for phylogenetic analysis of microbiomes. J Microbiol Methods 84:81–87
Taib N, Mangot JF, Domaizon I, Bronner G, Debroas D (2013) Phylogenetic affiliation of SSU rRNA genes generated by massively parallel sequencing: new insights into the freshwater protist diversity. PLoS ONE 8:e58950
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing Archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688
Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055
Massana R, DeLong EF, Pedros-Alio C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66:1777–1787
Abell GC, Revill AT, Smith C, Bissett AP, Volkman JK et al (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300
Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979
Winter C, Bouvier T, Weinbauer MG, Thingstad TF (2010) Trade-offs between competition and defense specialists among unicellular planktonic organisms: the “killing the winner” hypothesis revisited. Microbiol Mol Biol Rev 74:42–57
Sintes E, Bergauer K, De Corte D, Yokokawa T, Herndl GJ (2013) Archaeal amoA gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean. Environ Microbiol 15:1647–1658
Auguet JC, Casamayor EO (2013) Partitioning of Thaumarchaeota populations along environmental gradients in high mountain lakes. FEMS Microbiol Ecol 84:154–164
Restrepo-Ortiz CX, Auguet JC, Casamayor EO (2013) Targeting spatiotemporal dynamics of planktonic SAGMGC-1 and segregation of ammonia-oxidizing thaumarchaeota ecotypes by newly designed primers and quantitative polymerase chain reaction. Environ Microbiol 16:689–700
Mußmann M, Brito I, Pitcher A, Sinninghe Damste JS, Hatzenpichler R et al (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U S A 108:16771–16776
Pester M, Rattei T, Flechl S, Grongroft A, Richter A et al (2011) amoA-based consensus phylogeny of ammonia-oxidizing Archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539
Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661
Barberan A, Fernandez-Guerra A, Auguet JC, Galand PE, Casamayor EO (2011) Phylogenetic ecology of widespread uncultured clades of the kingdom Euryarchaeota. Mol Ecol 20:1988–1996
Frigaard NU, Martinez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439:847–850
Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL et al (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–590
Meng J, Xu J, Qin D, He Y, Xiao X et al (2014) Genetic and functional properties of uncultivated MCG Archaea assessed by metagenome and gene expression analyses. ISME J 8:650–659
Webster G, O’Sullivan LA, Meng Y, Williams AS, Sass AM et al (2015) Archaeal community diversity and abundance changes along a natural salinity gradient in estuarine sediments. FEMS Microbiol Ecol 91:1–18
Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M et al (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci U S A 103:2815–2820
Singh SK, Verma P, Ramaiah N, Chandrashekar AA, Shouche YS (2010) Phylogenetic diversity of archaeal 16S rRNA and ammonia monooxygenase genes from tropical estuarine sediments on the central west coast of India. Res Microbiol 161:177–186
Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA et al (2013) Predominant Archaea in marine sediments degrade detrital proteins. Nature 496:215–218
Acknowledgments
We thank P. Pineau, N. Lachaussée, M. Breret, F. Mornet, L. Beaugeard, J. Lavaud, and J. Jourde for the sampling. We thank A. Vellet, I. Louati, M. Breret, and C. Lavergne for their technical support during the experimentations and J.C. Auguet for providing us the map of the sampling location of the stations. This work was supported by a CNRS Program Ecosphère Continentale et Côtière (EC2CO, 2010–2012). The work of PE Galand was supported by the Agence Nationale de la Recherche (ANR) project MICADO (ANR-11JSV7-003-01).
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Supplementary Figure 1
Box plot of Shannon index from the three different sampling stations. A significant difference in diversity between two stations is marked with a star (*, p < 0.008) (GIF 23 kb)
Supplementary Figure 2
Ordination diagram from CCA of major active archaeal groups compared with environmental data (GIF 28 kb)
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Supplementary Table 1
Quality checked (QC) and Archaea affiliated sequences obtained for each sample from surface water collected monthly in the Charente estuary. Environmental parameters (temperature, salinity, pH, and Chla, ammonia and phosphates concentrations) associated to each point are presented. ND: not determined (XLS 43 kb)
Supplementary Table 2
Mean number of 16S rRNA sequences associated with each abundant OTU retrieved in the freshwater, mesohaline, and marine stations. ND: not determined (XLS 32 kb)
Supplementary Table 3
Monthly community structure at the subcluster level in Thaumarchaeota MGI. Number of OTUs were presented for each subgroup and number of sequences between brackets. ND: not determined (XLS 37 kb)
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Hugoni, M., Agogué, H., Taib, N. et al. Temporal Dynamics of Active Prokaryotic Nitrifiers and Archaeal Communities from River to Sea. Microb Ecol 70, 473–483 (2015). https://doi.org/10.1007/s00248-015-0601-z
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DOI: https://doi.org/10.1007/s00248-015-0601-z