Abstract
Nitrite-dependent anaerobic methane oxidation (N-DAMO) is a recently discovered process linking the global carbon and nitrogen cycles. This process was reported to be mediated by “Candidatus Methylomirabilis oxyfera”. To date, M. oxyfera-like bacteria have been detected in a limited number of freshwater habitats, but whether these bacteria occur in estuarine habitats is currently unknown. In this study, the distribution, diversity and abundance of M. oxyfera-like bacteria were studied in the sediment of the Jiaojiang Estuary of the East Sea (China). Both the 16S ribosomal RNA (rRNA) and pmoA genes confirmed the occurrence of M. oxyfera-like bacteria in the examined estuary. The recovered 16S rRNA gene sequences showed 91.5–97.2 % identity to the 16S rRNA gene of M. oxyfera, and the recovered pmoA gene sequences showed 85.1–95.4 % identity to the pmoA gene of M. oxyfera. Quantitative PCR further confirmed the occurrence of M. oxyfera-like bacteria in this estuary, with the abundance varying from 5.80 ± 0.28 × 104 to 8.35 ± 0.52 × 107 copies g (dry weight)−1. Correlation analysis indicated that the sediment organic content was the most important factor affecting the distribution of M. oxyfera-like bacterial communities in the examined sediments among the environmental factors investigated. This study demonstrated for the first time the existence of M. oxyfera-like bacteria in an estuarine environment and showed the correlations between the distribution of these bacteria and the estuarine environmental conditions.
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References
Deutzmann JS, Schink B (2011) Anaerobic oxidation of methane in sediments of Lake Constance, an oligotrophic freshwater lake. Appl Environ Microbiol 77:4429–4436
Du P, Liu JJ, Shen LD, Hu BL, Zeng JN, Chen QZ, Shou L, Liao YB (2012) Diversity of microorganisms in sediments of the Jiaojiang Estuary as estimated by Biolog and PCR-DGGE. Acta Sci Circumst 32:1436–1444
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Appl Environ Microbiol 27:2194–2200
Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M (2009) Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 75:3656–3662
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548
Han P, Gu JD (2013) A newly designed degenerate PCR primer based on pmoA gene for detection of nitrite-dependent anaerobic methane-oxidizing bacteria from different ecological niches. Appl Microbiol Biotechnol 97:10155–10162
Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11
Hu S, Zeng RJ, Burow LC, Lant P, Keller J, Yuan ZG (2009) Enrichment of denitrifying anaerobic methane oxidizing microorganisms. Environ Microbiol Rep 1:377–384
Hu BL, Shen LD, Du P, Zheng P, Xu XY, Zeng JN (2012) The influence of intense chemical pollution on the community composition, diversity and abundance of anammox bacteria in the Jiaojiang Estuary (China). PLoS ONE 7:3. doi:10.1371/journal.pone.0033826
Intergovernmental Panel on Climate Change (IPCC) (2001) Climate change 2001: the scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Juretschko S, Timmermann G, Schmid MC, Schleifer KH, Pommerening-Röser A, Koops HP, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051
Kampman C, Hendrickx TLG, Luesken FA, van Alen TA, Op den Camp HJM, Jetten MSM, Zeeman G, Buisman CJN, Temmink H (2012) Enrichment of denitrifying methanotrophic bacteria for application after direct low temperature anaerobic sewage treatment. J Hazard Mater 227–228:164–171
Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334
Kojima H, Tsutsumi M, Ishikawa K, Iwata T, Mußmann M, Fukui M (2012) Distribution of putative denitrifying methane oxidizing bacteria in sediment of a freshwater lake, Lake Biwa. Syst Appl Microbiol 35:233–238
Liu L, Ma DH (2005) Study of the situation of benthos in the sea area around the sewage outfall of Jiaonan chemical industry area. J Mar Sci 23:51–55
Luesken FA, Zhu B, van Alen TA, Butler MK, Rodriguez Diaz M, Song B, Op den Camp HJM, Jetten MSM, Ettwig KF (2011a) pmoA primers for detection of anaerobic methanotrophs. Appl Environ Microbiol 11:3877–3880
Luesken FA, van Alen TA, van der Biezen E, Frijters C, Toonen G, Kampman C, Hendrickx TLG, Zeeman G, Temmink H, Strous M, Op den Camp HJM, Jetten MSM (2011b) Diversity and enrichment of nitrite-dependent anaerobic methane oxidizing bacteria from wastewater sludge. Appl Microbiol Biotechnol 92:845–854
Luesken FA, Sánchez J, van Alen TA, Sanabria J, Op den Camp HJM, Jetten MS, Kartal B (2011c) Simultaneous nitrite-dependent anaerobic methane and ammonium oxidation process. Appl Environ Microbiol 77:6802–6807
Lüke C, Frenzel P (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77:6305–6309
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJ, Ettwig KF, Rijpstra WI, Schouten S, Damste JS, Op den Camp HJ, Jetten MS, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506
Shen LD, He ZF, Zhu Q, Chen DQ, Lou LP, Xu XY, Zheng P, Hu BL (2012) Microbiology, ecology and application of the nitrite-dependent anaerobic methane oxidation process. Front Microbiol 3:269. doi:10.3389/fmicb.2012.00269
Shen LD, Liu S, Zhu Q, Li XY, Cai C, Cheng DQ, Lou LP, Xu XY, Zheng P, Hu BL (2013a) Distribution and diversity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of the Qiantang River. Microb Ecol. doi:10.1007/s00248-013-0330-0
Shen LD, Liu S, Lou LP, Liu WP, Xu XY, Zheng P, Hu BL (2013b) Broad distribution of diverse anaerobic ammonium-oxidising bacteria in Chinese agricultural soils. Appl Environ Microbiol 79:6167–6172
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca
Wang Y, Zhu GB, Harhangi HR, Zhu BL, Jetten MSM, Yin CQ, Op den Camp HJ (2012) Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane oxidizing bacteria in a paddy soil. FEMS Microbiol Lett 336:79–88
Zhao YQ, Chen QZ, Zeng JN, Shou L, Gao AG, Liao YB (2009) Distribution characteristics of intertidal zone macrozoobenthos in autumn and winter in chemical industrial park and adjacent area, Jiaojiang Estuary. Acta Ecol Sin-China 29:1578–1586
Zhou SS, Shao LY, Yang HY, Wang C, Liu WP (2012) Residues and sources recognition of polychlorinated biphenyls in surface sediments of Jiaojiang Estuary, East China Sea. Mar Pollut Bull 64:539–545
Zhu BL, van Dijk G, Fritz C, Smolders AJP, Pol A, Jetten MSM, Ettwig KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol 78:8657–8665
Acknowledgments
The authors wish to thank the Natural Science Foundation (No. 51108408 and No. 41276109), the fund of Laboratory of Marine Ecosystem and Biogeochemistry (LMEB201007) and the Shanghai Tongji Gao Tingyao Environmental Science and Technology Development Foundation.
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Li-dong, S., Qun, Z., Shuai, L. et al. Molecular evidence for nitrite-dependent anaerobic methane-oxidising bacteria in the Jiaojiang Estuary of the East Sea (China). Appl Microbiol Biotechnol 98, 5029–5038 (2014). https://doi.org/10.1007/s00253-014-5556-3
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DOI: https://doi.org/10.1007/s00253-014-5556-3