Skip to main content
Log in

Acetate and sulphate as regulators of potential methane production in a tropical coastal lagoon

  • Sediments, Sec 2 • Physical and Biogeochemical Processes • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

We evaluated the influence of acetate and sulphate addition on methanogenesis in sediment layers of cores of different carbon and sulphate concentrations from the littoral region colonized by Typha domingensis Pers. (area 1) and from the limnetic region (area 2) of a tropical coastal lagoon separated from the sea by a sandbar. We hypothesized that area 1 presents a proportionally smaller potential methane production (PMP) on sulphate addition than area 2. We further hypothesized that acetate addition stimulates proportionally greater PMP in area 2 sediment layers than in area 1.

Materials and methods

The PMP rates were measured in sediment samples from three depths (0–2, 2–6, and 6–10 cm) in areas 1 and 2 for 89 days. The sediment incubations were prepared with additions of acetate (1 mM), sulphate (10 mM), and acetate plus sulphate (1 and 10 mM, respectively); the control treatment had no addition of acetate and/or sulphate. We also measured dissolved organic carbon (DOC), carbohydrates, and sulphate in the interstitial water.

Results and discussion

PMP responded differently to acetate and sulphate addition. In general, PMP in area 2 was proportionally more stimulated by the addition of acetate and less inhibited by the addition of sulphate. In the 0–2-cm layer, the addition of acetate did not stimulate PMP in relation to the control in area 1, reaching a rate of 376.11 nmol CH4 g−1 day−1. In area 2, PMP was 5-fold higher in relation to the control, reaching 5.4 nmol CH4 g−1 day−1. Contrarily, in the 6–10-cm layer, sulphate addition inhibited PMP by 127.8-fold in relation to the control in area 1, reaching 0.6 nmol CH4 g−1 day−1. In area 2, PMP decreased 3.2-fold in relation to the control, reaching a value of 3.7 nmol CH4 g−1 day−1. These results agreed with the higher amounts of carbohydrates and lower amounts of sulphate in area 1 in the experiment beginning.

Conclusions

Acetate and sulphate are effective PMP regulators in the sediment of two areas of a tropical coastal lagoon. Acetate increased PMP more in area 2, due to the lower sediment carbon availability. In contrast, sulphate decreased PMP more in area 1, due to the lower sulphate availability. The metabolic responses of methanogens and sulphate-reducing bacteria to natural and anthropogenic changes in carbon and sulphate availability are important for understanding the functioning of continental aquatic ecosystems, especially in scenarios of global climate change.

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

Similar content being viewed by others

References

  • Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72

    Article  CAS  Google Scholar 

  • Ambühl H, Bührer H (1975) Zur Technik der Entnahme ungestörter Grossproben von Seesediment: ein verbessertes Bohrlot. Schweiz Z Hydrol 37:175–186

    Google Scholar 

  • American Public Health Association-APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. APHA, Washington DC

    Google Scholar 

  • Baldwin DS, Mitchell A (2012) Impact of sulfate pollution on anaerobic biogeochemical cycles in a wetland sediment. Water Res 46:965–974

    Article  CAS  Google Scholar 

  • Bergman I, Klarqvist M, Nilsson M (2000) Seasonal variation in rates of methane production from peat of various botanical origins: effects of temperature and substrate quality. FEMS Microbiol Ecol 33:181–189

    Article  CAS  Google Scholar 

  • Bhullar GS, Edwards PJ, Venterink HO (2013) Variation in the plant-mediated methane transport and its importance for methane emission from intact wetland peat mesocosms. J Plant Ecol 6:298–304

    Article  Google Scholar 

  • Bhullar GS, Edwards PJ, Olde Venterink H (2014) Influence of different plant species on methane emissions from soil in a restored Swiss wetland. PLoS One 9:e89588. https://doi.org/10.1371/journal.pone.0089588

    Article  CAS  Google Scholar 

  • Bousquet P, Ciais P, Miller JB, Dlugokencky EJ, Hauglustaine DA, Prigent C, Van der Werf GR, Peylin P, Brunke E-G, Carouge C, Langenfelds RL, Lathière J, Papa F, Ramonet M, Schmidt M, Steele LP, Tyler SC, White J (2006) Contribution of anthropogenic and natural sources to atmospheric methane variability. Nature 443:439–443

    Article  CAS  Google Scholar 

  • Bozelli RL, Esteves FA, Farjalla VF, Marinho CC, Caliman A (2004) Relatório anual do projeto ECOLagoas. Laboratório de Limnologia/UFRJ, Rio de Janeiro

    Google Scholar 

  • Bridgham SD, Cadillo-Quiroz H, Keller JK, Zhuang Q (2013) Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob Chang Biol 19:1325–1346

    Article  Google Scholar 

  • Caliman A, Carneiro LS, Santangelo JM, Guariento RD, Pires AP, Suhett AL, Quesado LB, Siqueira VS, Fonte ES, Lopes PM, Sanches LF, Azevedo FD, Marinho CC, Bozelli RL, Esteves FA, Farjalla VF (2010) Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Braz J Bio 70:803–814

    Article  CAS  Google Scholar 

  • Chambers LG, Reddy KR, Osborne TZ (2011) Short-term response of carbon cycling to salinity pulses in a freshwater wetland. Soil Sci Soc Am J 75:2000–2007

    Article  CAS  Google Scholar 

  • Chuang P, Young MB, Dale AW, Miller LG, Herrera-Silveira JA, Paytan A (2016) Methane and sulfate dynamics in sediments from mangrove-dominated tropical coastal lagoons, Yucatán, Mexico. Biogeosciences 13:2981–3001

    Article  CAS  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. Wiley-Interscience, 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 

  • Dalcin Martins P, Hoyt DW, Bansal S, Mills CT, Tfaily M, Tangen BA, Finocchiaro RG, Johnston MD, McAdams BC, Solensky MJ, Smith GJ, Chin Y-P, Wilkins MJ (2017) Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands. Glob Chang Biol 23:3107–3120

    Article  Google Scholar 

  • Ding WX, Cai ZC, Tsuruta H (2005) Plant species effects on methane emissions from freshwater marshes. Atmos Environ 39:3199–3207

    Article  CAS  Google Scholar 

  • Esteves FA, Caliman A (2011) Águas continentais: características do meio, compartimentos e suas comunidades. In: Esteves FA (coord) Fundamentos de Limnologia, 3rd edn. Interciência, Rio de Janeiro, pp 113–118

    Google Scholar 

  • Esteves FA, Caliman A, Santangelo JM, Guariento RD, Farjalla VF, Bozelli RL (2008) Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Braz J Biol 68:967–981

    Article  CAS  Google Scholar 

  • Esteves FA, Ishii II, Camargo AFM (1984) Pesquisas limnológicas em 14 lagoas do litoral do Estado do Rio de Janeiro. In: Lacerda LD, Araujo DSD, Cerqueira R, Turcq B (eds) Restingas: origem, estrutura e processos. CEUFF, Niterói, pp 443–454

  • Esteves FA (1998) Lagoas costeiras: origem, funcionamento e possibilidades de manejo. In: Esteves FA (ed) Ecologia das lagoas costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ). NUPEM-UFRJ, Rio de Janeiro, pp 63–87

    Google Scholar 

  • Fonseca ALS, Marinho CC, Esteves FA (2017) Potential methane production associated with aquatic macrophytes detritus in a tropical coastal lagoon. Wetlands 37:763–771

    Article  Google Scholar 

  • Fonseca ALS, Minello M, Marinho CC, Esteves FA (2004) Methane concentration in water column and in pore water of a coastal lagoon (Cabiúnas Lagoon, Macaé, RJ, Brazil). Braz Arch Biol Technol 47:301–308

    Article  Google Scholar 

  • Golterman HL, Clymo RS, Ohnstad MAM (1978) Methods of physical and chemical analysis of freshwaters. Blackwell, Oxford

    Google Scholar 

  • Jerman V, Danevčič T, Mandic-Mulec I (2017) Methane cycling in a drained wetland soil profile. J Soils Sediments 17:1874–1882

    Article  CAS  Google Scholar 

  • Junk WJ, Piedade MTF, Lourival R, Wittmann F, Kandus P, Lacerda LD, Bozelli RL, Esteves FA, Nunes da Cunha C, Maltchik L, Schöngart J, Schaeffer-Novelli Y, Agostinho AA (2014) Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquatic Conserv: Mar Freshw Ecosyst 24:5–22

    Article  Google Scholar 

  • Libes S (2009) Introduction to marine biogeochemistry, 2nd edn. Academic Press, Oxford

    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 

  • Lovley DR, Klug MJ (1983) Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Appl Environ Microbiol 45:187–192

    CAS  Google Scholar 

  • Marinho CC, Meirelles-Pereira F, Gripp AR, Guimarães CC, Esteves FA, Bozelli RL (2010) Aquatic macrophytes drive sediment stoichiometry and the suspended particulate organic carbon composition of a tropical coastal lagoon. Acta Limnol Bras 22:208–217

    Article  Google Scholar 

  • Martens CS, Klump JV (1984) Biogeochemical cycling in an organic-rich coastal marine basin 4. An organic carbon budget for sediments dominated by sulfate reduction and methanogenesis. Geochim Cosmochim Acta 48:1987–2004

    Article  CAS  Google Scholar 

  • Myhre G, Shindell D, Bréon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, NY, USA, pp 659–740

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

    CAS  Google Scholar 

  • Ozuolmez D, Na H, Lever MA, Kjeldsen KU, Jørgensen BB, Plugge CM (2015) Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence? Front Microbiol 6:492

    Article  Google Scholar 

  • Panosso RF, Attayde JL, Muehe D (1998) Morfometria das lagoas Imboassica, Cabiúnas, Comprida e Carapebus: implicações para seu funcionamento e manejo. In: Esteves FA (ed) Ecologia das lagoas costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ). NUPEM/UFRJ, Rio de Janeiro, pp 91–105

    Google Scholar 

  • Pester M, Knorr K-H, Friedrich MW, Wagner M, Loy A (2012) Sulfate-reducing microorganisms in wetlands—fameless actors in carbon cycling and climate change. Front Microbiol 3(72). https://doi.org/10.3389/fmicb.2012.00072

  • Rothman E, Bouchard V (2007) Regulation of carbon processes by macrophyte species in a Great Lakes coastal wetland. Wetlands 27:1134–1143

    Article  Google Scholar 

  • Santos AM, Esteves FA (2004) Influence of water level fluctuation on the mortality and aboveground biomass of the aquatic macrophyte Eleocharis interstincta (VAHL) Roemer et Schults. Braz Arch Biol Technol 47:281–290

    Article  Google Scholar 

  • Schönheit P, Kristjansson JK, Thauer RK (1982) Kinetic mechanism for the ability of sulfate reducers to out-compete methanogens for acetate. Arch Microbiol 132:285–288

    Article  Google Scholar 

  • Segarra KEA, Comerford C, Slaughter J, Joye SB (2013) Impact of electron acceptor availability on the anaerobic oxidation of methane in coastal freshwater and brackish wetland sediments. Geochim Cosmochim Acta 115:15–30

    Article  CAS  Google Scholar 

  • Strangmann A, Bashan Y, Giani L (2008) Methane in pristine and impaired mangrove soils and its possible effect on establishment of mangrove seedlings. Biol Fertil Soils 44:511–519

    Article  CAS  Google Scholar 

  • Thomaz SM, Esteves FA (2011) Comunidades de macrófitas aquáticas. In: Esteves FA (coord) Fundamentos de Limnologia, 3rd edn. Interciência, Rio de Janeiro, pp 461–521

    Google Scholar 

  • Vizza C, West WE, Jones SE, Hart JA, Lamberti GA (2017) Regulators of coastal wetland methane production and responses to simulated global change. Biogeosciences 14:431–446

    Article  CAS  Google Scholar 

  • Ward DM, Winfrey MR (1985) Interactions between methanogenic and sulfate-reducing bacteria in sediments. Adv Aquat Microbiol 3:141–179

    Google Scholar 

  • Yavitt JB, Lang GE (1990) Methane production in contrasting wetland sites: response to organic-chemical components of peat and to sulfate reduction. Geomicrobiol J 8:27–46

    Article  CAS  Google Scholar 

  • Zak D, Reuter H, Augustin J, Shatwell T, Barth M, Gelbrecht J, McInnes RJ (2015) Changes of the CO2 and CH4 production potential of rewetted fens in the perspective of temporal vegetation shifts. Biogeosci Discuss 12:2455–2468

    Article  CAS  Google Scholar 

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

    Chapter  Google Scholar 

Download references

Acknowledgements

We thank the two anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions.

Funding

We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to André Luiz dos Santos Fonseca.

Additional information

Responsible editor: Lionel Denis

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

dos Santos Fonseca, A.L., Marinho, C.C. & de Assis Esteves, F. Acetate and sulphate as regulators of potential methane production in a tropical coastal lagoon. J Soils Sediments 19, 2604–2612 (2019). https://doi.org/10.1007/s11368-019-02249-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-019-02249-y

Keywords

Navigation