Skip to main content

Advertisement

SpringerLink
Log in

How do Elevated CO2 and Nitrogen Addition Affect Functional Microbial Community Involved in Greenhouse Gas Flux in Salt Marsh System

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Salt marshes are unique ecosystem of which a microbial community is expected to be affected by global climate change. In this study, by using T-RFLP analysis, quantitative PCR, and pyrosequencing, we comprehensively analyzed the microbial community structure responding to elevated CO2 (eCO2) and N addition in a salt marsh ecosystem subjected to CO2 manipulation and N addition for about 3 years. We focused on the genes of microbes relevant to N-cycling (denitrification and nitrification), CH4-flux (methanogens and methanotrophs), and S-cycling (sulfate reduction) considering that they are key functional groups involved in the nutrient cycle of salt marsh system. Overall, this study suggests that (1) eCO2 and N addition affect functional microbial community involved in greenhouse gas flux in salt marsh system. Specifically, the denitrification process may be facilitated, while the methanogenesis may be impeded due to the outcompeting of sulfate reduction by eCO2 and N. This implies that future global change may cause a probable change in GHGs flux and positive feedback to global climate change in salt marsh; (2) the effect of eCO2 and N on functional group seems specific and to contrast with each other, but the effect of single factor would not be compromised but complemented by combination of two factors. (3) The response of functional groups to eCO2 and/or N may be directly or indirectly related to the plant community and its response to eCO2 and/or N. This study provides new insights into our understanding of functional microbial community responses to eCO2 and/or N addition in a C3/C4 plant mixed salt marsh system.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81:169–193

    Article  Google Scholar 

  2. Bowen JL, Ward BB, Morrison HG, Hobbie JE, Valiela I, Deegan LA, et al (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5:1540–1548

    Article  PubMed  PubMed Central  Google Scholar 

  3. Seyler LM, McGuinness LM, Kerkhof LJ (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME J 8:1534–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Weber CF, Zak DR, Hungate BA, Jackson RB, Vilgalys R, Evans RD, et al (2011) Response of soil cellulolytic fungal communities to elevated atmospheric CO2 are complex and variable across five ecosystems. Environ. Microbiol. 13:2778–2793

    Article  CAS  PubMed  Google Scholar 

  5. Gedan KB, Silliman BR, Bertness MD (2009) Centuries of human-driven change in salt marsh ecosystems. Annu. Rev. Mar. Sci. 1:117–141

    Article  Google Scholar 

  6. Langely JA, McKee KI, Cahoon DR, Cherry JA, Megonigal JP (2008) Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc Nat Aca Sci 106:6182–6186

    Article  Google Scholar 

  7. Kirwan ML, Mudd SM (2012) Response of salt-marsh carbon accumulation to climate change. Nature 489:550–553

    Article  CAS  PubMed  Google Scholar 

  8. Caffrey JM, Murrell JC, Wigand C, McKinney RA (2007) Effect of nutrient loading on biogeochemical and microbial processes in a New England salt marsh. Biogeochem 82:251–264

    Article  CAS  Google Scholar 

  9. Graham SA, Mendelssohn IA (2010) Multiple levels of nitrogen applied to an oligohaline marsh identify a plant community response sequence to eutrophication. Mar. Ecol. Prog. Ser. 417:73–82

    Article  Google Scholar 

  10. Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 level limited by nitrogen-induced plant species shift. Nature 466:96–99

    Article  CAS  PubMed  Google Scholar 

  11. Bowen JL, Crump BC, Deegan LA, Hobbie JE (2009) Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. ISME J 3:924–934

    Article  CAS  PubMed  Google Scholar 

  12. Bragazza L, Buttler A, Habermacher J, Brancaleoni L, Gerdo R, Fritze H, et al (2012) High nitrogen deposition alters the decomposition of bog plant litter and reduces carbon accumulation. Glob Change Biol 18:1163–1172

    Article  Google Scholar 

  13. Chen Z, Luo X, Hu R, Wu M, Wu J, Wei W (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb. Ecol. 60:850–861

    Article  CAS  PubMed  Google Scholar 

  14. Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Change Biol 18:1918–1927

    Article  Google Scholar 

  15. Stiehl-Braun PA, Hartmann AA, Kandeler E, Buchmann N, Niklaus PA (2011) Interactive effects of drought and N fertilization on the spatial distribution of methane assimilation in grassland soils. Glob Change Biol 17:2629–2639

    Article  Google Scholar 

  16. Xiong J, He Z, Shi S, Kent A, Deng Y, Wu L, Van Nostrand JD, Zhou J (2015) Elevated CO2 shifts the functional structure and metabolic potentials of soil microbial communities in a C4 agroecosystem. Sci Rep 5:9316

    Article  PubMed  PubMed Central  Google Scholar 

  17. McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software, Gleneden Beach

    Google Scholar 

  18. Langley JA, Sigrist MV, Duls J, Cahoon DR, Lynch JC, Megonigal JP (2009) Global change and marsh elevation dynamics: experimenting where land meets sea and biology meets geology. Smithson. Contrib. Mar. Sci. 38:391–400

    Article  Google Scholar 

  19. Palmer K, Biasi C, Horn MA (2012) Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J 6:1058–1077

    Article  CAS  PubMed  Google Scholar 

  20. Kelly JJ, Peterson E, Winkelman J, Walter TJ, Rier ST, Tuchman NC (2013) Elevated atmospheric CO2 impacts abundance and diversity of nitrogen cycling functional genes in soil. Microb. Ecol. 65:394–404

    Article  CAS  PubMed  Google Scholar 

  21. Hunger S, Schmidt O, Hilgarth M, Horn MA, Kolb S, Conrad R, Drake HL (2011) Competing formate- and carbon dioxide utilizing prokaryotes in an anoxic methane-emitting fen soil. Appl. Environ. Microbiol. 77:3773–3785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Degelmann DM, Borken W, Drake HL, Kolb S (2010) Different atmospheric methane-oxidizing communities in European beech and Norway spruce soils. Appl. Environ. Microbiol. 76:3228–3235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bowen JL, Byrnes JEK, Weisman D, Colaneri C (2013) Functional gene pyrosequencing and network analysis: an approach to examine the response of denitrifying bacteria to increased nitrogen supply in salt marsh sediments. Front. Microbiol. 4:342. doi:10.3389/fmicb.2013.00342

    Article  PubMed  PubMed Central  Google Scholar 

  24. White KP, Langley JA, Cahoon DR, Megonigal JP (2012) C3 and C4 biomass allocation responses to elevated CO2 and nitrogen: contrasting resource capture strategies. Estuar Coast 35:1028–1035

    Article  CAS  Google Scholar 

  25. van Groenigen KJ, Osenberg GW, Hungate BA (2011) Increased soil emissions of potent greenhouse gases under increased atmospheric CO2. Nature 475:214–216

    Article  PubMed  Google Scholar 

  26. Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641

    Article  PubMed  Google Scholar 

  27. Lee JA, Francis CA (2016) Spatiotemporal characterization of San Francisco Bay denitrifying communities: a comparison of nirK and nirS diversity and abundance. Microb. Ecol. doi:10.1007/s00248-016-0865-y

    PubMed Central  Google Scholar 

  28. Wang H-T, Su J-Q, Zheng T-L, Yang X-R (2014) Impacts of vegetation, tidal process, and depth on the activities, abundances, and community compositions of denitrifiers in mangrove sediment. Appl Microbiol Biotech 98:9375–9387

    Article  CAS  Google Scholar 

  29. Yuan Q, Liu P, Lu Y (2012) Differential responses of nirK- and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environ. Microbiol. Rep. 4:113–122

    Article  CAS  PubMed  Google Scholar 

  30. Bañeras L, Ruiz-Rueda O, López-Flores R, Quintana X, Hallin S (2012) The role of plant type and salinity in the selection for the denitrifying community structure in the rhizosphere of wetland vegetation. Int. Microbiol. 15:89–99

    PubMed  Google Scholar 

  31. Hamersley MR, Howes BL (2005) Coupled nitrification-denitrification measured in situ in a Spartina alterniflora marsh with a 15NH4 + tracer. Mar. Ecol. Prog. Ser. 299:123–135

    Article  CAS  Google Scholar 

  32. Peng X, Yando E, Hildebrand E, Dwyer C, Kearney A, Waciega A, et al (2013) Differential responses of ammonia-oxidizing archaea and bacteria to long-term fertilization in a New England salt marsh. Front in Microbiol 3:445–455

    Article  Google Scholar 

  33. Caffrey JM, Hollibaugh JT, Bano N, Haskins J (2010) Effects of upwelling on short-term variability in microbial and biogeochemical processes in estuarine sediments from Elkhorn Slough, California, USA. Aquat. Microb. Ecol. 58:261–271

    Article  Google Scholar 

  34. Long X, Chen C, Xu Z, Oren R, He J-Z (2012) Abundance and community structure of ammonia-oxidizing bacteria and archaea in a temperate forest ecosystem under ten-years elevated CO2. Soil Biol. Biochem. 46:163–171

    Article  CAS  Google Scholar 

  35. Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ. Microbiol. 14:993–1008

    Article  CAS  PubMed  Google Scholar 

  36. Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PLE (2008) Soil type links microbial colonization of rice roots to methane emission. Glob Change Biol 14:657–669

    Article  Google Scholar 

  37. Zeleke J, Sheng Q, Wang J-G, Huang M-Y, Xia F, Wu J-H, Quan Z (2013) Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Front. Microbiol. 4:243. doi:10.3389/fmicb.2013.00243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Aronson EL, Helliker BR (2010) Methane flux in non-wetland soils in response to nitrogen addition: a meta-analysis. Ecology 91:3242–3251

    Article  CAS  PubMed  Google Scholar 

  39. Chmura GL, Kellman L, van Ardenne L, Guntenspergen GR (2016) Greenhouse gas fluxes from salt marshes exposed to chronic nutrient enrichment. PLoS One 11:e0149937

    Article  PubMed  PubMed Central  Google Scholar 

  40. Irvine IC, Vivanco L, Bentley PN, Martiny JBH (2012) The effect of nitrogen enrichment on C1-cycling microorganisms and methane flux in salt marsh sediments. Front. Microbiol. 3:90. doi:10.3389/fmicb.2012.00090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Jang I, Lee SH, Zho KD, Kang H (2011) Methane concentrations and methanotrophic community structure influence the response of soil methane oxidation to nitrogen content in a temperate forest. Soil Biol. Biochem. 43:620–627

    Article  CAS  Google Scholar 

  42. Kolb S, Carbrera A, Kammann C, Kämpfer P, Conrad R, Jäckel U (2005) Quantitative impact of CO2 enriched atmosphere on abundances of methanotrophic bacteria in a meadow soil. Biol. Fertil. Soils 41:337–342

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by NRF (2011-0030040) and SGER (2016R1D1A1A02937049).

Author information

Authors and Affiliations

  1. School of Civil and Environmental Engineering, Yonsei University, Seoul, 120-749, South Korea

    Seung-Hoon Lee & Hojeong Kang

  2. Smithsonian Environmental Research Center, Washington, DC, 20013, USA

    Patrick J. Megonigal

Authors
  1. Seung-Hoon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick J. Megonigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hojeong Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hojeong Kang.

Electronic Supplementary Material

ESM 1

(DOCX 69 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, SH., Megonigal, P.J. & Kang, H. 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 (2017). https://doi.org/10.1007/s00248-017-0960-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0960-8

Keywords

Search

Navigation