Skip to main content

Advertisement

Log in

Methylococcaceae are the dominant active aerobic methanotrophs in a Chinese tidal marsh

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Although coastal marshes are net carbon sinks, they are net methane sources. Aerobic methanotrophs in coastal marsh soils are important methane consumers, but their activity and populations are poorly characterized. DNA stable-isotope probing followed by sequencing was used to determine how active methanotrophic populations differed in the main habitats of a Chinese coastal marsh. These habitats included mudflat, native plant-dominated, and alien plant-dominated habitats. Methylococcaceae was the most active methanotroph family across four habitats. Abundant methylotroph sequences, including methanotrophs and non-methane-oxidizing methylotrophs (Methylotenera and Methylophaga), constituted 50–70% of the 16S rRNA genes detected in the labeled native plant-dominated and mudflat soils. Methylotrophs were less abundant (~ 20%) in labeled alien plant-dominated soil, suggesting less methane assimilation into the target community or a different extent of carbon cross-feeding. Canonical correspondence analysis indicated a significant correlation between the active bacterial communities and soil properties (salinity, organic carbon, total nitrogen, pH, and available phosphorus). Importantly, these results highlight how changing vegetation or soil features in coastal marshes may change their resident active methanotrophic populations, which will further influence methane cycling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adam P (1990) Saltmarsh ecology. Cambridge University Press, New York

    Book  Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Angenent LT, Kelley ST, Amand AS, Pace NR, Hernandez MT (2005) Molecular identification of potential pathogens in water and air of a hospital therapy pool. Proc Natl Acad Sci U S A 102:4860–4865

    Article  CAS  Google Scholar 

  • Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6:221–231

    Article  Google Scholar 

  • Beck DAC, Kalyuzhnaya MG, Malfatti S, Tringe SG, Glavina Del Rio T, Ivanova N, Lidstrom ME, Chistoserdova L (2013) A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae. PeerJ 1:e23

    Article  Google Scholar 

  • Bertness MD (1985) Fiddler crab regulation of Spartina alterniflora production on a New England salt marsh. Ecology 66:1042–1055

    Article  Google Scholar 

  • Bowman JP, Sly LI, Nichols PD, Hayward AC (1993) Revised taxonomy of the methanotrophs: description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43:735–753

    Article  Google Scholar 

  • Bremner JM, Jenkinson DS (1960) Determination of organic carbon in soil. Eur J Soil Sci 11:394–402

    Article  CAS  Google Scholar 

  • Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33

    Article  CAS  Google Scholar 

  • Chen Y, Dumont MG, McNamara NP, Chamberlain PM, Bodrossy L, Stralis-Pavese N, Murrell JC (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol 10:446–459

    Article  CAS  Google Scholar 

  • Chistoserdova L (2011) Methylotrophy in a lake: from metagenomics to single-organism physiology. Appl Environ Microbiol 77:4705–4711

    Article  CAS  Google Scholar 

  • Chistoserdova L (2015) Methylotrophs in natural habitats: current insights through metagenomics. Appl Microbiol Biotechnol 99:5763–5779

    Article  CAS  Google Scholar 

  • Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292

    Article  CAS  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074

    CAS  Google Scholar 

  • Deng Y, Cui X, Lüke C, Dumont M (2013) Aerobic methanotroph diversity in Riganqiao peatlands on the Qinghai-Tibetan Plateau. Environ Microbiol Rep 5:566–574

    Article  CAS  Google Scholar 

  • Deng Y, Cui X, Dumont M (2016) Identification of active aerobic methanotrophs in plateau wetlands using DNA stable isotope probing. FEMS Microbiol Lett 363:fnw168

    Article  Google Scholar 

  • Deng Y, Liu Y, Dumont M, Conrad R (2017) Salinity affects the composition of the aerobic methanotroph community in alkaline lake sediments from the Tibetan Plateau. Microb Ecol 73:101–110

    Article  Google Scholar 

  • Doronina NV, Krauzova VI, Trotsenko YA (1997) Methylophaga limanica sp. nov.: a new species of moderately halophilic, aerobic, methylotrophic bacteria. Microbiology 66:434–439

    CAS  Google Scholar 

  • Dumont MG, Lüke C, Deng Y, Frenzel P (2014) Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN. Front Microbiol 5(34)

  • Dumont MG, Murrell JC (2005) Community-level analysis: key genes of aerobic methane oxidation. Environ Microbiol, Methods in Enzymology, ed Leadbetter JR. 397:413–427

  • Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y, Wang J, Mountain BW, Crowe MA, Weatherby TM, Bodelier PLE, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–U818

    Article  CAS  Google Scholar 

  • Dunfield PF, Belova SE, Vorob'ev AV, Cornish SL, Dedysh SN (2010) Methylocapsa aurea sp. nov., a facultative methanotroph possessing a particulate methane monooxygenase, and emended description of the genus Methylocapsa. Int J Syst Evol Microbiol 60:2659–2664

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  Google Scholar 

  • Fradet DT, Tavormina PL, Orphan VJ (2016) Members of the methanotrophic genus Methylomarinum inhabit inland mud pots. PeerJ 4:e2116

    Article  Google Scholar 

  • Ghosh A, Dey N, Bera A, Tiwari A, Sathyaniranjan KB, Chakrabarti K, Chattopadhyay D (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarban, India. Saline Systems 6(1)

  • Gupta V, Smemo KA, Yavitt JB, Basiliko N (2012) Active methanotrophs in two contrasting North American peatland ecosystems revealed using DNA-SIP. Microb Ecol 63:438–445

    Article  CAS  Google Scholar 

  • Han DF, Link H, Liesack W (2017) Response of Methylocystis sp strain SC2 to salt stress: physiology, global transcriptome and amino acid profiles. Appl Environ Microbiol 83(14)

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439

    CAS  Google Scholar 

  • Hirayama H, Abe M, Miyazaki M, Nunoura T, Furushima Y, Yamamoto H, Takai K (2014) Methylomarinovum caldicuralii gen. nov., sp. nov., a moderately thermophilic methanotroph isolated from a shallow submarine hydrothermal system, and proposal of the family Methylothermaceae fam. nov. Int J Syst Evol Microbiol 64:989–999

    Article  CAS  Google Scholar 

  • Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida Coastal Everglades marsh-mangrove-seagrass salinity gradient. Microb Ecol 59:284–295

    Article  Google Scholar 

  • IPCC (2014) In: Core writing team, Pachauri RK, Meyer LA (eds) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, pp. 151

  • Kip N, Fritz C, Langelaan ES, Pan Y, Bodrossy L, Pancotto V, Jetten MSM, Smolders AJP, den Camp HJMO (2012) Methanotrophic activity and diversity in different Sphagnum magellanicum dominated habitats in the southernmost peat bogs of Patagonia. Biogeosciences 9:47–55

    Article  CAS  Google Scholar 

  • Kirwan ML, Guntenspergen GR, D'Alpaos A, Morris JT, Mudd SM, Temmerman S (2010) Limits on the adaptability of coastal marshes to rising sea level. Geophys Res Lett 37:L23401

    Article  Google Scholar 

  • Knief C (2015) Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front Microbiol 6:1346

    Article  Google Scholar 

  • Kolb S, Knief C, Stubner S, Conrad R (2003) Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microb 69:2423–2429

    Article  CAS  Google Scholar 

  • Krause SMB, Johnson T, Samadhi Karunaratne Y, Fu Y, Beck DAC, Chistoserdova L, Lidstrom ME (2017) Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions. Proc Natl Acad Sci U S A 114:358–363

    Article  CAS  Google Scholar 

  • Lee SH, Megonigal PJ, Kang H (2017) How do elevated CO2 and nitrogen addition affect functional microbial community involved in greenhouse gas flux in salt marsh system. Microb Ecol 74:670–680

    Article  CAS  Google Scholar 

  • Lidstrom ME (2006) Aerobic methylotrophic prokaryotes. The Prokaryotes, (Springer), pp 618–634

  • Livesley SJ, Andrusiak SM (2012) Temperate mangrove and salt marsh sediments are a small methane and nitrous oxide source but important carbon store. Estuar Coast Shelf Sci 97:19–27

    Article  CAS  Google Scholar 

  • Lueders T, Wagner B, Claus P, Friedrich MW (2004) Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol 6:60–72

    Article  CAS  Google Scholar 

  • Lüke C, Frenzel P (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77:6305–6309

    Article  Google Scholar 

  • Mudd SM, Howell SM, Morris JT (2009) Impact of dynamic feedbacks between sedimentation, sea-level rise, and biomass production on near-surface marsh stratigraphy and carbon accumulation. Estuar Coast Shelf S 82:377–389

    Article  CAS  Google Scholar 

  • Murrell JC (2010) The aerobic methane oxidizing bacteria (methanotrophs). Handbook of hydrocarbon and lipid microbiology, (Springer), pp 1953–1966

  • Nellemann, Christian; Corcoran, Emily; Duarte, Carlos M.; De Young, Cassandra; Fonseca, Luciano E.; and Grimsdith, Gabriel (2010), "Blue carbon: the role of healthy oceans in binding carbon". Center for Coastal and Ocean Mapping 132

  • Neufeld JD, Schäfer H, Cox MJ, Boden R, McDonald IR, Murrell JC (2007b) Stable-isotope probing implicates Methylophaga spp and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J 1:480–491

    Article  CAS  Google Scholar 

  • Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, Murrell JC (2007a) DNA stable-isotope probing. Nat Protocols 2:860–866

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RG, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) Vegan: community ecology package. R Package Version 2.2–0

  • Poffenbarger HJ, Needelman BA, Megonigal JP (2011) Salinity influence on methane emissions from tidal marshes. Wetlands 31:831–842

    Article  Google Scholar 

  • Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, den Camp HJMO (2007) Methanotrophy below pH1 by a new Verrucomicrobia species. Nature 450:874–879

    Article  CAS  Google Scholar 

  • Prieur D, Troussellier M, Romana A, Chamrouxd S, Meveld G, Baleuxb B (1987) Evolution of bacterial communities in the Gironde estuary (France) according to a salinity gradient. Estuar Coast Shelf Sci 24:95–108

    Article  Google Scholar 

  • Qin P, Zhong CX (1992) Applied studies on Spartina. Ocean Press 26:s160–s169

    Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  Google Scholar 

  • Saidi-Mehrabad A (2014) Characterization of aerobic methane oxidizing bacteria in oil sands tailings ponds. MSc thesis. University of Calgary

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541

    Article  CAS  Google Scholar 

  • Shiau YJ, Cai Y, Lin YT, Jia Z, Chiu CY (2018) Community structure of active aerobic methanotrophs in red mangrove (Kandelia obovata) soils under different frequency of tides. Microb Ecol 75:761–770

    Article  Google Scholar 

  • Tang L, Gao Y, Li B, Wang Q, Wang CH, Zhao B (2014) Spartina alterniflora with high tolerance to salt stress changes vegetation pattern by outcompeting native species. Ecosphere 5:1–18

    Article  CAS  Google Scholar 

  • Tavormina PL, Ussler W, Joye SB, Harrison BK, Orphan VJ (2010) Distributions of putative aerobic methanotrophs in diverse pelagic marine environments. ISME J 4:700–710

    Article  Google Scholar 

  • Wang C, Liu H (2014) The impact of Spartina alterniflora expansion on vegetation landscapes in the Yancheng tidal flat wetland. Resources Sci 36:2413–2422

    Google Scholar 

  • Xiang J, Liu D, Ding W, Yuan J, Lin Y (2015) Invasion chronosequence of Spartina alterniflora on methane emission and organic carbon sequestration in a coastal salt marsh. Atmos Environ 112:72–80

    Article  CAS  Google Scholar 

  • Xu X, Zou X, Cao L, Zhamangulova N, Zhao Y, Tang D, Liu D (2014) Seasonal and spatial dynamics of greenhouse gas emissions under various vegetation covers in a coastal saline wetland in southeast China. Ecol Eng 73:469–477

    Article  Google Scholar 

  • Yuan J, Ding W, Liu D, Xiang J, Lin Y (2014) Methane production potential and methanogenic archaea community dynamics along the Spartina alterniflora invasion chronosequence in a coastal salt marsh. Appl Microbiol Biotechnol 98:1817–1829

    Article  CAS  Google Scholar 

  • Yuan J, Ding W, Liu D, Kang H, Freeman C, Xiang J, Lin Y (2015) Exotic Spartina alterniflora invasion alters ecosystem–atmosphere exchange of CH4 and N2O and carbon sequestration in a coastal salt marsh in China. Glob Change Biol 21:1567–1580

    Article  Google Scholar 

  • Zhang Y, Ding W, Cai Z, Valerie P, Han F (2010b) Response of methane emission to invasion of Spartina alterniflora and exogenous N deposition in the coastal salt marsh. Atmos Environ 44:4588–4594

    Article  CAS  Google Scholar 

  • Zhang Y, Ding W, Luo J, Donnison A (2010a) Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biol and Biochem 42:1712–1720

    Article  CAS  Google Scholar 

  • Zhang RS, Shen YM, Lu LY, Yan SG, Wang YH, Li JL, Zhang ZL (2004) Formation of Spartina alterniflora salt marshes on the coast of Jiangsu Province. China Ecol Eng 23:95–105

    Article  CAS  Google Scholar 

  • Zuo P, Zhao S, Ca L, Wang C, Liang Y (2012) Distribution of Spartina spp. along China’s coast. Ecol Eng 40:160–166

    Article  Google Scholar 

Download references

Funding

This work was supported by the Natural Science Foundation of Jiangsu Province, China [grant number BK20140923 and BK20181386], the National Natural Science Foundation of China [grant number 41401075], and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenhui Zhong.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Robert Duran

Electronic supplementary material

Figure S1

Changes in the copy number of pmoA genes in soils of four marsh habitats (MF: mudflat, PA: Phragmites australis-, SS: Suaeda salsa-, and SA: Spartina alterniflora-dominated) incubated with 13CH4 or 12CH4 for 6 days. Error bars represent standard deviations (n = 3). (PNG 31 kb)

High resolution image (EPS 599 kb)

Figure S2

Bacterial 16S rRNA gene T-RFLP analysis of the DNA recovered from the CsCl gradient fractions. The three panels on the upper left of the figure, MF-1, MF-2, and MF-3 represent three replications of the heavy fractions of 13CH4-labeled mudflat (MF) soils, while panels in their left represent three replications of the light fractions of the 12CH4-incubated MF soil. The same principles were applied to Phragmites australis- (PA), Suaeda salsa- (SS), and Spartina alterniflora- (SA) dominated soils. The numbers accompanying the arrows point to each T-RF peak indicates the respective T-RF length (bp). The associated CsCl buoyant density (g ml-1) is listed at the center-top of each panel. (PNG 234 kb)

High resolution image (EPS 2415 kb)

Figure S3

Relative abundance of the major 16S rRNA gene-derived clusters in the Sanger sequencing datasets that were retrieved from the heavy fractions of the labeled soils (density = ~ 1.74 g ml–1). (PNG 145 kb)

High resolution image (EPS 733 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deng, Y., Gui, Q., Dumont, M. et al. Methylococcaceae are the dominant active aerobic methanotrophs in a Chinese tidal marsh. Environ Sci Pollut Res 26, 636–646 (2019). https://doi.org/10.1007/s11356-018-3560-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3560-3

Keywords

Navigation