Skip to main content
Log in

Methane production potential and methanogenic archaea community dynamics along the Spartina alterniflora invasion chronosequence in a coastal salt marsh

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Invasion by the exotic species Spartina alterniflora, which has high net primary productivity and superior reproductive capacity compared with native plants, has led to rapid organic carbon accumulation and increased methane (CH4) emission in the coastal salt marsh of China. To elucidate the mechanisms underlying this effect, the methanogen community structure and CH4 production potential as well as soil organic carbon (SOC), dissolved organic carbon, dissolved organic acids, methylated amines, aboveground biomass, and litter mass were measured during the invasion chronosequence (0–16 years). The CH4 production potential in the S. alterniflora marsh (range, 2.94–3.95 μg kg−1 day−1) was significantly higher than that in the bare tidal mudflat. CH4 production potential correlated significantly with SOC, acetate, and trimethylamine concentrations in the 0–20 cm soil layer. The abundance of methanogenic archaea also correlated significantly with SOC, and the dominant species clearly varied with S. alterniflora-driven SOC accumulation. The acetotrophic Methanosaetaceae family members comprised a substantial proportion of the methanogenic archaea in the bare tidal mudflat while Methanosarcinaceae family members utilized methylated amines as substrates in the S. alterniflora marsh. Ordination analysis indicated that trimethylamine concentration was the primary factor inducing the shift in the methanogenic archaea composition, and regressive analysis indicated that the facultative family Methanosarcinaceae increased linearly with trimethylamine concentration in the increasingly sulfate-rich salt marsh. Our results indicate that increased CH4 production during the S. alterniflora invasion chronosequence was due to increased levels of the non-competitive substrate trimethylamine and a shift in the methanogenic archaea community.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams CA, Andrews JE, Jickells T (2012) Nitrous oxide and methane fluxes vs. carbon, nitrogen and phosphorous burial in new intertidal and saltmarsh sediments. Sci Total Environ 434:240–251

    Article  CAS  PubMed  Google Scholar 

  • An SQ, Gu BH, Zhou CF, Wang ZS, Deng ZF, Zhi YB, Li HL, Chen L, Yu DH, Liu YH (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res 47:183–191

    Article  Google Scholar 

  • Angeles OR, Johnson SE, Buresh RJ (2006) Soil solution sampling for organic acids in rice paddy soils. Soil Sci Soc Am J 70:48–56

    Article  CAS  Google Scholar 

  • Banning N, Brock F, Fry JC, Parkes RJ, Hornibrook ERC, Weightman AJ (2005) Investigation of the methanogen population structure and activity in a brackish lake sediment. Environ Microbiol 7:947–960

    Article  CAS  PubMed  Google Scholar 

  • Boone DR (1991) Ecology of methanogenesis. In: Rogers JE, Whitman WB (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes. ASM, Washington, pp 57–70

    Google Scholar 

  • Braak CT, Smilauer P (2002) CANOCO reference manual and user’s guide to Canoco for Windows: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, New York, USA

  • Buckley DH, Baumgartner LK, Visscher PT (2008) Vertical distribution of methane metabolism in microbial mats of the Great Sippewissett Salt Marsh. Environ Microbiol 10:967–977

    Article  CAS  PubMed  Google Scholar 

  • Cahyani VR, Murase J, Ikeda A, Taki K, Asakawa S, Kimura M (2008) Bacterial communities in iron mottles in the plow pan layer in a Japanese rice field: estimation using PCR-DGGE and sequencing analyses. Soil Sci Plant Nutr 54:711–717

    Article  CAS  Google Scholar 

  • Carter MR (1993) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, Florida

    Google Scholar 

  • Cavalieri AJ, Huang AH (1981) Accumulation of proline and glycinebetaine in Spartina alterniflora Loisel. in response to NaCl and nitrogen in the marsh. Oecologia 49:224–228

    Article  Google Scholar 

  • Cheng X, Peng R, Chen J, Luo Y, Zhang Q, An S, Chen J, Li B (2007) CH4 and N2O emissions from Spartina alterniflora and Phragmites australis in experimental mesocosms. Chemosphere 68:420–427

    Article  CAS  PubMed  Google Scholar 

  • Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC (2003) Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem Cycles 17, GB1111. doi:10.1029/2002gb001917

    Article  Google Scholar 

  • Choi Y, Wang Y (2004) Dynamics of carbon sequestration in a coastal wetland using radiocarbon measurements. Global Biogeochem Cycles 18, GB4016. doi:10.1029/2004GB002261

    Article  Google Scholar 

  • Chung C, Zhuo R, Xu G (2004) Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecol Eng 23:135–150

    Article  Google Scholar 

  • Conrad R (1989) Control of methane production in terrestrial ecosystems. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. Dahlem Konferenzen. Wiley, Chichester, pp 39–58

    Google Scholar 

  • Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752

    Article  CAS  Google Scholar 

  • Conrad R, Klose M, Noll M (2009) Functional and structural response of the methanogenic microbial community in rice field soil to temperature change. Environ Microbiol 11:1844–53

    Article  CAS  PubMed  Google Scholar 

  • Dacey JW, King GM, Wakeham SG (1987) Factors controlling emission of dimethylsulphide from salt marshes. Nature 330:643–645

    Article  CAS  Google Scholar 

  • Dacey JWH, Wakeham SG (1986) Oceanic dimethylsulfide—production during zooplankton grazing on phytoplankton. Science 233:1314–1316

    Article  CAS  PubMed  Google Scholar 

  • Fey A, Conrad R (2000) Effect of temperature on carbon and electron flow and on the archaeal community in methanogenic rice field soil. Appl Environ Microbiol 66:4790–4797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franklin MJ, Wiebe WJ, Whitman WB (1988) Populations of methanogenic bacteria in a Georgia salt-marsh. Appl Environ Microbiol 54:1151–1157

    CAS  PubMed Central  PubMed  Google Scholar 

  • Froelich P, Klinkhammer G, Maa B, Luedtke N, Heath GR, Cullen D, Dauphin P, Hammond D, Hartman B, Maynard V (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta 43:1075–1090

    Article  CAS  Google Scholar 

  • Galand PE, Fritze H, Conrad R, Yrjala K (2005) Pathways for methanogenesis and diversity of methanogenic archaea in three boreal peatland ecosystems. Appl Environ Microbiol 71:2195–8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Galand PE, Fritze H, Yrjala K (2003) Microsite-dependent changes in methanogenic populations in a boreal oligotrophic fen. Environ Microbiol 5:1133–1143

    Article  PubMed  Google Scholar 

  • Garcia-Maldonado JQ, Bebout BM, Celis LB, Lopez-Cortes A (2012) Phylogenetic diversity of methyl-coenzyme M reductase (mcrA) gene and methanogenesis from trimethylamine in hypersaline environments. Int Microbiol 15:33–41

    CAS  PubMed  Google Scholar 

  • Godin A, McLaughlin JW, Webster KL, Packalen M, Basiliko N (2012) Methane and methanogen community dynamics across a boreal peatland nutrient gradient. Soil Biol Biochem 48:96–105

    Article  CAS  Google Scholar 

  • Hori T, Noll M, Igarashi Y, Friedrich MW, Conrad R (2007) Identification of acetate-assimilating microorganisms under methanogenic conditions in anoxic rice field soil by comparative stable isotope probing of RNA. Appl Environ Microbiol 73:101–109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jetten MSM, Stams AJM, Zehnder AJB (1990) Acetate threshold values and acetate activating enzymes in methanogenic bacteria. FEMS Microbiol Ecol 73:339–344

    Article  CAS  Google Scholar 

  • Jetten MSM, Stams AJM, Zehnder AJB (1992) Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Rev 88:181–197

    Article  CAS  Google Scholar 

  • Juottonen H, Galand PE, Tuittila ES, Laine J, Fritze H, Yrjala K (2005) Methanogen communities and bacteria along an ecohydrological gradient in a northern raised bog complex. Environ Microbiol 7:1547–57

    Article  CAS  PubMed  Google Scholar 

  • Kelley CA, Poole JA, Tazaz AM, Chanton JP, Bebout BM (2012) Substrate limitation for methanogenesis in hypersaline environments. Astrobiology 12:89–97

    Article  CAS  PubMed  Google Scholar 

  • King GM (1984) Utilization of hydrogen, acetate, and “noncompetitive”; substrates by methanogenic bacteria in marine sediments. Geomicrobiol J 3:275–306

    CAS  Google Scholar 

  • King GM, Klug MJ, Lovley DR (1983) Metabolism of acetate, methanol, and methylated amines in intertidal sediments of Lowes Cove, Maine. Appl Environ Microbiol 45:1848–1853

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koizumi Y, Takii S, Nishino M, Nakajima T (2003) Vertical distributions of sulfate–reducing bacteria and methane–producing archaea quantified by oligonucleotide probe hybridization in the profundal sediment of a mesotrophic lake. FEMS Microbiol Ecol 44:101–108

    Article  CAS  PubMed  Google Scholar 

  • Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Ding W, Jia Z, Cai Z (2012) The impact of dissolved organic carbon on the spatial variability of methanogenic archaea communities in natural wetland ecosystems across China. Appl Microbiol Biotechnol 96:253–63

    Article  CAS  PubMed  Google Scholar 

  • Liu DY, Ding WX, Jia ZJ, Cai ZC (2011) Relation between methanogenic archaea and methane production potential in selected natural wetland ecosystems across China. Biogeosciences 8:329–338

    Article  CAS  Google Scholar 

  • 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 

  • Lu YH, Lueders T, Friedrich MW, Conrad R (2005) Detecting active methanogenic populations on rice roots using stable isotope probing. Environ Microbiol 7:326–336

    Article  CAS  PubMed  Google Scholar 

  • Lyimo TJ, Pol A, Jetten MS, den Camp HJ (2009) Diversity of methanogenic archaea in a mangrove sediment and isolation of a new Methanococcoides strain. FEMS Microbiol Lett 291:247–53

    Article  CAS  PubMed  Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Merila P, Galand PE, Fritze H, Tuittila ES, Kukko-Oja K, Laine J, Yrjala K (2006) Methanogen communities along a primary succession transect of mire ecosystems. FEMS Microbiol Ecol 55:221–9

    Article  CAS  PubMed  Google Scholar 

  • Montoya L, Lozada-Chavez I, Amils R, Rodriguez N, Marin I (2011) The sulfate-rich and extreme saline sediment of the ephemeral tirez lagoon: a biotope for acetoclastic sulfate-reducing bacteria and hydrogenotrophic methanogenic archaea. Int J Microbiol 2011:753758

    Article  PubMed Central  PubMed  Google Scholar 

  • Mori K, Iino T, Suzuki K, Yamaguchi K, Kamagata Y (2012) Aceticlastic and NaCl-requiring methanogen "Methanosaeta pelagica" sp. nov., isolated from marine tidal flat sediment. Appl Environ Microbiol 78:3416–23

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111

    Article  CAS  PubMed  Google Scholar 

  • Noll M, Klose M, Conrad R (2010) Effect of temperature change on the composition of the bacterial and archaeal community potentially involved in the turnover of acetate and propionate in methanogenic rice field soil. FEMS Microbiol Ecol 73:215–25

    Article  CAS  PubMed  Google Scholar 

  • Oremland RS, Marsh LM, Polcin S (1982) Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 296:143–145

    Article  CAS  Google Scholar 

  • Oremland RS, Polcin S (1982) Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44:1270–1276

    CAS  PubMed Central  PubMed  Google Scholar 

  • Parkes RJ, Brock F, Banning N, Hornibrook ERC, Roussel EG, Weightman AJ, Fry JC (2012) Changes in methanogenic substrate utilization and communities with depth in a salt-marsh, creek sediment in southern England. Estuar Coast Shelf Sci 96:170–178

    Article  Google Scholar 

  • Parkes RJ, Cragg BA, Banning N, Brock F, Webster G, Fry JC, Hornibrook E, Pancost RD, Kelly S, Knab N, Jorgensen BB, Rinna J, Weightman AJ (2007) Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments (Skagerrak, Denmark). Environ Microbiol 9:1146–61

    Article  CAS  PubMed  Google Scholar 

  • Purdy KJ, Munson MA, Cresswell-Maynard T, Nedwell DB, Embley TM (2003) Use of 16S rRNA-targeted oligonucleotide probes to investigate function and phylogeny of sulphate-reducing bacteria and methanogenic archaea in a UK estuary. FEMS Microbiol Ecol 44:361–371

    Article  CAS  PubMed  Google Scholar 

  • Qin P, Zhong C (1992) Applied studies on Spartina. Ocean Press, China, Beijing

    Google Scholar 

  • Reed R, Chudek J, Foster R, Stewart W (1984) Osmotic adjustment in cyanobacteria from hypersaline environments. Arch Microbiol 138:333–337

    Article  CAS  Google Scholar 

  • Rhodes D, Hanson A (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Biol 44:357–384

    Article  CAS  Google Scholar 

  • Rooney-Varga JN, Giewat MW, Duddleston KN, Chanton JP, Hines ME (2007) Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands. FEMS Microbiol Ecol 60:240–51

    Article  CAS  PubMed  Google Scholar 

  • van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  • Vitousek PM, Dantonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Wang XC, Lee C (1994) Sources and distribution of aliphatic-amines in salt-marsh sediment. Org Geochem 22:1005–1021

    Article  CAS  Google Scholar 

  • Watanabe T, Kimura M, Asakawa S (2009) Distinct members of a stable methanogenic archaeal community transcribe mcrA genes under flooded and drained conditions in Japanese paddy field soil. Soil Biol Biochem 41:276–285

    Article  CAS  Google Scholar 

  • Westermann P, Ahring BK, Mah RA (1989) Threshold acetate concentrations for acetate catabolism by aceticlastic methanogenic bacteria. Appl Environ Microbiol 55:514–515

    CAS  PubMed Central  PubMed  Google Scholar 

  • Winfrey MR, Ward DM (1983) Substrates for sulfate reduction and methane production in intertidal sediments. Appl Environ Microbiol 45:193–199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu Y, Lee C, Hwang S (2005) Analysis of community structures in anaerobic processes using a quantitative real-time PCR method. Water Sci Technol 52:85–91

    CAS  PubMed  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 

  • Zhang Y, Ding W, Cai Z, Valerie P, Han F (2010a) 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 (2010b) Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biol Biochem 42:1712–1720

    Article  CAS  Google Scholar 

  • Zhou C, An S, Deng Z, Yin D, Zhi Y, Sun Z, Zhao H, Zhou L, Fang C, Qian C (2009) Sulfur storage changed by exotic Spartina alterniflora in coastal saltmarshes of China. Ecol Eng 35:536–543

    Article  Google Scholar 

  • Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogens: ecology, physiology, biochemistry & genetics. Chapman & Hall, New York, pp 128–206

    Chapter  Google Scholar 

Download references

Acknowledgment

This work was supported by the strategic priority research program—Climate Change: Carbon Budget and Relevant Issues of the Chinese Academy of Sciences (XDA05020501), the National Basic Research Program of China (2012CB417102), and the Natural Science Foundation of China (41171190, 41001045, and 41001173).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weixin Ding.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yuan, J., Ding, W., Liu, D. et al. 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 (2014). https://doi.org/10.1007/s00253-013-5104-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5104-6

Keywords

Navigation