Abstract
Thaumarchaeota and Bathyarchaeota (formerly named Miscellaneous Crenarchaeotal Group, MCG) are globally occurring archaea playing potential roles in nitrogen and carbon cycling, especially in marine benthic biogeochemical cycle. Information on their distributional and compositional patterns could provide critical clues to further delineate their physiological and biochemical characteristics. Profiles of thaumarchaeotal and the total archaeal community in the northern South China Sea surface sediments revealed a successively transitional pattern of Thaumarchaeota composition using MiSeq sequencing. Shallow-sea sediment enriched phylotypes decreased gradually along the slope from estuarine and coastal marine region to the deep-sea, while deep-sea sediment enriched phylotypes showed a trend of increasing. Proportion of Thaumarchaeota within the total archaea increased with seawater depth. Phylotypes enriched in shallow- and deep-sea sediments were affiliated to OTUs originated from similar niches, suggesting that physiological adaption not geographical distance shaped the distribution of Thaumarchaeota lineages. Quantitative PCR also depicted a successive decrease of thaumarchaeotal 16S rRNA gene abundance from the highest at shallow-sea sites E708S and E709S (2.57 × 106 and 2.73 × 106 gene copies/g of dry sediment) to the lowest at deep-sea sites E525S and E407S (1.97 × 106 and 2.14 × 106 gene copies/g of dry sediment). Both of the abundance fractions of Bathyarchaeota subgroups (including subgroups 1, 6, 8, 10, 13, 15, 17, and ungrouped Bathyarchaeota) and the total Bathyarchaeota in the total archaea showed a negative distribution to seawater depth. Partitioned distribution of Bathyarchaeota fraction in the total archaea is documented for the first time in this study, and the shallow- and deep-sea Bathyarchaeota could account for 17.8 and 0.8%, respectively, on average. Subgroups 6 and 8, enriched subgroups in shallow-sea sediments, largely explained this partitioned distribution pattern according to seawater depth. Their prevalence in shallow-sea and suboxic estuarine sediments rather than deep-sea sediments hints that their metabolic properties of carbon metabolism are adapted to carbon substrates in these environments.
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References
Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431(7005):181–184. https://doi.org/10.1038/nature02850
Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sorensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs KU (2006) Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci U S A 103(10):3846–3851. https://doi.org/10.1073/pnas.0600035103
Bouskill NJ, Eveillard D, Chien D, Jayakumar A, Ward BB (2012) Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environ Microbiol 14(3):714–729. https://doi.org/10.1111/j.1462-2920.2011.02623.x
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245–252. https://doi.org/10.1038/nrmicro1852
Cai H, Jiao N (2008) Diversity and abundance of nitrate assimilation genes in the northern South China Sea. Microb Ecol 56(4):751–764. https://doi.org/10.1007/s00248-008-9394-7
Callahan J, Dai MH, Chen RF, Li XL, Lu ZM, Huang W (2004) Distribution of dissolved organic matter in the Pearl River estuary, China. Mar Chem 89(1–4):211–224. https://doi.org/10.1016/j.marchem.2004.02.013
Cao H, Hong Y, Li M, Gu J-D (2011) Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River estuary to the South China Sea. Antonie Van Leeuwenhoek 100(4):545–556
Cao H, Hong Y, Li M, Gu J-D (2012) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl Microbiol Biotechnol 94(1):247–259. https://doi.org/10.1007/s00253-011-3636-1
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624. https://doi.org/10.1038/ismej.2012.8
Chen ZQ, Li Y, Pan JM (2004) Distributions of colored dissolved organic matter and dissolved organic carbon in the Pearl River estuary, China. Cont Shelf Res 24(16):1845–1856. https://doi.org/10.1016/j.csr.2004.06.011
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89(12):5685–5689. https://doi.org/10.1073/pnas.89.12.5685
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350(6259):434–438
Fillol M, Sànchez-Melsió A, Gich F, Borrego CM (2015) Diversity of Miscellaneous Crenarchaeotic Group archaea in freshwater karstic lakes and their segregation between planktonic and sediment habitats. FEMS Microbiol Ecol 91(4). doi:https://doi.org/10.1093/femsec/fiv020
Fillol M, Auguet J-C, Casamayor EO, Borrego CM (2016) Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J 10(3):665–677. https://doi.org/10.1038/ismej.2015.143
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(41):14683–14688. https://doi.org/10.1073/pnas.0506625102
Francis CA, Beman JM, Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1(1):19–27. https://doi.org/10.1038/ismej.2007.8
Gagen EJ, Huber H, Meador T, Hinrichs K-U, Thomm M (2013) Novel cultivation-based approach to understanding the Miscellaneous Crenarchaeotic Group (MCG) archaea from sedimentary ecosystems. Appl Environ Microbiol 79(20):6400–6406. https://doi.org/10.1128/aem.02153-13
He Y, Li M, Perumal V, Feng X, Fang J, Xie J, Sievert SM, Wang F (2016) Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1(6):16035. https://doi.org/10.1038/nmicrobiol.2016.35
Hong J-K, Kim H-J, Cho J-C (2014) Novel PCR primers for the archaeal phylum Thaumarchaeota designed based on the comparative analysis of 16S rRNA gene sequences. PLoS One 9(5):e96197. https://doi.org/10.1371/journal.pone.0096197
Hou MH, Xiong JB, Wang K, Ye XS, Ye R, Wang Q, Hu CJ, Zhang DM (2014) Communities of sediment ammonia-oxidizing bacteria along a coastal pollution gradient in the East China Sea. Mar Pollut Bull 86(1–2):147–153. https://doi.org/10.1016/j.marpolbul.2014.07.031
Huang X, Huang L, Yue W (2003) The characteristics of nutrients and eutrophication in the Pearl River estuary, South China. Mar Pollut Bull 47(1):30–36
Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, Nealson KH, Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microbiol 69(12):7224–7235. https://doi.org/10.1128/aem.69.12.7224-7235.2003
Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ERM, Pearson A (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci U S A 103(17):6442–6447. https://doi.org/10.1073/pnas.0510157103
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, Kirchman DL, Weinbauer MG, Luo T, Chen F, Azam F (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8(8):593–599. https://doi.org/10.1038/nrmicro2386
Kim BK, Jung M-Y, Yu DS, Park S-J, Oh TK, Rhee S-K, Kim JF (2011) Genome sequence of an ammonia-oxidizing soil archaeon, “Candidatus Nitrosoarchaeum koreensis” MY1. J Bacteriol 193(19):5539–5540. https://doi.org/10.1128/jb.05717-11
Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543–546. https://doi.org/10.1038/nature03911
Kubo K, Lloyd KG, Biddle JF, Amann R, Teske A, Knittel K (2012) Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J 6(10):1949–1965. https://doi.org/10.1038/ismej.2012.37
Lazar CS, Biddle JF, Meador TB, Blair N, Hinrichs K-U, Teske AP (2015) Environmental controls on intragroup diversity of the uncultured benthic archaea of the miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA). Environ Microbiol 17(7):2228–2238. https://doi.org/10.1111/1462-2920.12659
Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs K-U, Teske AP (2016) Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol 18(4):1200–1211. https://doi.org/10.1111/1462-2920.13142
Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Li PY, Xie BB, Zhang XY, Qin QL, Dang HY, Wang XM, Chen XL, Yu J, Zhang YZ (2012) Genetic structure of three fosmid-fragments encoding 16S rRNA genes of the Miscellaneous Crenarchaeotic Group (MCG): implications for physiology and evolution of marine sedimentary archaea. Environ Microbiol 14(2):467–479. https://doi.org/10.1111/j.1462-2920.2011.02637.x
Li M, Hong Y, Cao H, Gu J-D (2013) Community structures and distribution of anaerobic ammonium oxidizing and nirS-encoding nitrite-reducing bacteria in surface sediments of the South China Sea. Microb Ecol 66(2):281–296. https://doi.org/10.1007/s00248-012-0175-y
Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jorgensen BB (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496(7444):215–218. https://doi.org/10.1038/nature12033
Lösekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microbiol 73(10):3348–3362
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 8(3):650–659. https://doi.org/10.1038/ismej.2013.174
Mosier AC, Allen EE, Kim M, Ferriera S, Francis CA (2012) Genome sequence of “Candidatus Nitrosopumilus salaria” BD31, an ammonia-oxidizing archaeon from the San Francisco Bay estuary. J Bacteriol 194(8):2121–2122. https://doi.org/10.1128/jb.00013-12
Motulsky H (1999) Analyzing data with GraphPad prism. GraphPad Software Incorporated, San Diego
Park S-J, Ghai R, Martin-Cuadrado A-B, Rodriguez-Valera F, Chung W-H, Kwon K, Lee J-H, Madsen EL, Rhee S-K (2014) Genomes of two new ammonia-oxidizing archaea enriched from deep marine sediments. PLoS One 9(5):e96449. https://doi.org/10.1371/journal.pone.0096449
Reed DW, Fujita Y, Delwiche ME, Blackwelder DB, Sheridan PP, Uchida T, Colwell FS (2002) Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin. Appl Environ Microbiol 68(8):3759–3770
Schauer R, Roy H, Augustin N, Gennerich H-H, Peters M, Wenzhoefer F, Amann R, Meyerdierks A (2011) Bacterial sulfur cycling shapes microbial communities in surface sediments of an ultramafic hydrothermal vent field. Environ Microbiol 13(10):2633–2648. https://doi.org/10.1111/j.1462-2920.2011.02530.x
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60
Seyler LM, McGuinness LM, Kerkhof LJ (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME J 8(7):1534–1543. https://doi.org/10.1038/ismej.2014.15
Singh SK, Verma P, Ramaiah N, Anil CA, 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(3):177–186. https://doi.org/10.1016/j.resmic.2010.01.008
Spang A, Poehlein A, Offre P, Zumbraegel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T, Boehm C, Schmid M, Galushko A, Hatzenpichler R, Weinmaier T, Daniel R, Schleper C, Spieck E, Streit W, Wagner M (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14(12):3122–3145. https://doi.org/10.1111/j.1462-2920.2012.02893.x
Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101. https://doi.org/10.1146/annurev-micro-092611-150128
Stieglmeier M, Klingl A, Alves RJE, Rittmann SKMR, Melcher M, Leisch N, Schleper C (2014) Nitrososphaera viennensis gen. nov., sp nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. Int J Syst Evol Microbiol 64:2738–2752. https://doi.org/10.1099/ijs.0.063172-0
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(11):5066–5072. https://doi.org/10.1128/aem.66.11.5066-5072.2000
Tourna M, Stieglmeier M, Spang A, Koenneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108(20):8420–8425. https://doi.org/10.1073/pnas.1013488108
Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach AL (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65(10):4375–4384
Webster G, Rinna J, Roussel EG, Fry JC, Weightman AJ, Parkes RJ (2010) Prokaryotic functional diversity in different biogeochemical depth zones in tidal sediments of the Severn Estuary, UK, revealed by stable-isotope probing. FEMS Microbiol Ecol 72(2):179–197. https://doi.org/10.1111/j.1574-6941.2010.00848.x
Xie W, Zhang C, Zhou X, Wang P (2014) Salinity-dominated change in community structure and ecological function of archaea from the lower Pearl River to coastal South China Sea. Appl Microbiol Biotechnol 98(18):7971–7982. https://doi.org/10.1007/s00253-014-5838-9
Yu T, Liang Q, Niu M, Wang F (2017) High occurrence of Bathyarchaeota (MCG) in the deep-sea sediments of South China Sea quantified using newly designed PCR primers. Environ Microbiol Rep 9:374–382. https://doi.org/10.1111/1758-2229.12539
Zhang W, Saren G, Li T, Yu X, Zhang L (2010) Diversity and community structure of archaea in deep subsurface sediments from the tropical western Pacific. Curr Microbiol 60(6):439–445. https://doi.org/10.1007/s00284-009-9562-0
Zhang QF, Tang FY, Zhou YJ, Xu JR, Chen HP, Wang MK, Laanbroek HJ (2015) Shifts in the pelagic ammonia-oxidizing microbial communities along the eutrophic estuary of Yong River in Ningbo City, China. Front Microbiol 6. doi:https://doi.org/10.3389/fmicb.2015.01180
Acknowledgements
We thank Ms. Kelly Lau for her technical help and Prof. Xiangzhen Li and his colleagues at Chengdu Institute of Biology, Chinese Academy of Sciences for their support on MiSeq sequencing and related bioinformatics analysis.
Funding
This research was supported by a PhD studentship from The University of Hong Kong (ZZ) and RGC GRF grant no. 701913 and TRS T21-711/16-R (J-DG); National Natural Science Foundation of China No. 31500076 (GXZ).
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Zhou, Z., Zhang, GX., Xu, YB. et al. Successive transitory distribution of Thaumarchaeota and partitioned distribution of Bathyarchaeota from the Pearl River estuary to the northern South China Sea. Appl Microbiol Biotechnol 102, 8035–8048 (2018). https://doi.org/10.1007/s00253-018-9147-6
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DOI: https://doi.org/10.1007/s00253-018-9147-6