Skip to main content
SpringerLink
Log in

Filamentous green algae Spirogyra regulates methane emissions from eutrophic rivers

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

Abstract

Excessive growth of filamentous green algae in rivers has attracted much attention due to their functional importance to primary production and carbon cycling. However, comprehensive knowledge of how filamentous green algae affect carbon cycling, especially the CH4 emissions from river ecosystems, remains limited. In this study, incubation experiments were conducted to examine the factors regulating CH4 emissions from a eutrophic river with dense growth of filamentous green algae Spirogyra through combinations of biogeochemical, molecular biological, and stable carbon isotope analyses. Results showed that although water dissolved oxygen (DO) in the algae+sediment (A+S) incubation groups increased up to 19 mg L−1, average CH4 flux of the groups was 13.09 μmol m−2 day−1, nearly up to two times higher than that from sediments without algae (S groups). The significant increase of sediment CH4 oxidation potential and methanotroph abundances identified the enhancing sediment CH4 oxidation during Spirogyra bloom. However, the increased water CH4 concentration was consistent with depleted water \( {\delta}^{13}{\mathrm{C}}_{{\mathrm{C}\mathrm{H}}_4} \) and decreased apparent fractionation factor (αapp), suggesting the important contribution of Spirogyra to the oxic water CH4 production. It can thus be concluded that high DO concentration during the algal bloom promoted the CH4 consumption by enhancing sediment CH4 oxidation, while algal-linked oxic water CH4 production as a major component of water CH4 promoted the CH4 emissions from the river. Our study highlights the regulation of Spirogyra in aquatic CH4 fluxes and will help to estimate accurately CH4 emissions from eutrophic rivers with dense blooms of filamentous green algae.

Graphical abstract

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
Fig. 5

Similar content being viewed by others

References

  • Angle JC, Morin TH, Solden LM, Narrowe AB, Smith GJ, Borton MA, Reysanchez C, Daly RA, Mirfenderesgi G, Hoyt DW, Riley WJ, Miller CS, Bohrer G, Wrighton KC (2017) Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. Nat Commun 8:1567

    Article  CAS  Google Scholar 

  • Bastviken D, Ejlertsson J, Tranvik L (2002) Measurement of methane oxidation in lakes: a comparison of methods. Environ Sci Technol 36:3354–3361

    Article  CAS  Google Scholar 

  • Bastviken D, Cole J, Pace M, Tranvik L (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem Cycles 18:GB4009

    Article  CAS  Google Scholar 

  • Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrichprast A (2011) Freshwater methane emissions offset the continental carbon sink. Science 331:50–50

    Article  CAS  Google Scholar 

  • Bian R, Komiya T, Shimaoka T, Chai X, Sun Y (2019) Simulative analysis of vegetation on CH4 emission from landfill cover soils: combined effects of root-water uptake, root radial oxygen loss, and plant-mediated CH4 transport. J Clean Prod 234:18–26

    Article  CAS  Google Scholar 

  • Bogard MJ, Giorgio PA, Boutet L, Chaves MC, Prairie YT, Merante A, Derry AM (2014) Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nat Commun 5:5350

    Article  CAS  Google Scholar 

  • Cadieux SB, White JR, Sauer PE, Peng Y, Goldman AE, Pratt LM (2016) Large fractionations of C and H isotopes related to methane oxidation in Arctic lakes. Geochim Cosmochim Ac 187:141–155

    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. 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 

  • Crawford JT, Stanley EH, Spawn SA, Finlay JC, Loken LC, Striegl RG (2014) Ebullitive methane emissions from oxygenated wetland streams. Global Change Biol 20:3408–3422

    Article  Google Scholar 

  • Crowe SA, Katsev S, Leslie K, Sturm A, Magen C, Nomosatryo S, Pack MA, Kessler JD, Reeburgh WS, Roberts JA, Gonzalez LA, Douglas Haffner G, Mucci A, Sundby B, Fowle DA (2010) The methane cycle in ferruginous Lake Matano. Geobiology 9:61–78

    Article  CAS  Google Scholar 

  • Den Heyer C, Kalff J (1998) Organic matter mineralization rates in sediments: a within-and among-lake study. Limnol Oceanogr 43:695–705

    Article  Google Scholar 

  • Dodla SK, Wang JJ, Delaune RD, Breitenbeck G (2009) Carbon gas production under different electron acceptors in a freshwater marsh soil. Chemosphere 76:517–522

    Article  CAS  Google Scholar 

  • Donis D, Flury S, Stockli A, Spangenberg JE, Vachon D, Mcginnis DF (2017) Full-scale evaluation of methane production under oxic conditions in a mesotrophic lake. Nat Commun 8:1661

    Article  CAS  Google Scholar 

  • Dutta MK, Mukherjee R, Jana TK, Mukhopadhyay S (2015) Biogeochemical dynamics of exogenous methane in an estuary associated to a mangrove biosphere. The Sundarbans, NE Coast of India. Mar Chem 170:1–10

    Article  CAS  Google Scholar 

  • Ferrón S, Ho DT, Johnson ZI, Huntley ME (2012) Air–water fluxes of N2O and CH4 during microalgae (Staurosira sp.) cultivation in an open raceway pond. Environ Sci Technol 46:10842–10848

    Article  CAS  Google Scholar 

  • Flores-Moya A, Costas E, Bañares-España E, García-Villada L, Altamirano M, López-Rodas V (2005) Adaptation of Spirogyra insignis (Chlorophyta) to an extreme natural environment (sulphureous waters) through preselective mutations. New Phytol 166:655–661

    Article  Google Scholar 

  • Flury S, Glud RN, Premke K, McGinnis DF (2015) Effect of sediment gas voids and ebullition on benthic solute exchange. Environ Sci Technol 49:10413–10420

    Article  CAS  Google Scholar 

  • Friedrich MW (2005) Methyl-coenzyme M reductase genes: unique functional markers for methanogenic and anaerobic methane-oxidizing Archaea. Method Enzymol 397:428–442

    Article  CAS  Google Scholar 

  • Fritz C, Pancotto VA, Elzenga JTM, Visser EJW, Grootjans AP, Pol A, Iturraspe R, Roelofs JGM, Smolders AJP (2011) Zero methane emission bogs: extreme rhizosphere oxygenation by cushion plants in Patagonia. New Phytol 190:398–408

    Article  Google Scholar 

  • Grasset C, Abril G, Mendonca R, Roland F, Sobek S (2019) The transformation of macrophytes-derived organic matter to methane relates to plant water and nutrient contents. Limnol Oceanogr 64:1737–1749

    Article  CAS  Google Scholar 

  • Grossart H, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. PNAS 108:19657–19661

    Article  CAS  Google Scholar 

  • Guillemette F, Mccallister SL, Giorgio PA (2013) Differentiating the degradation dynamics of algal and terrestrial carbon within complex natural dissolved organic carbon in temperate lakes. J Geophys Res Biogeosci 118:963–973

    Article  CAS  Google Scholar 

  • He S, Malfatti S, Mcfarland JW, Anderson F, Pati A, Huntemann M, Tremblay J, Glavina del Rio T, Waldrop MP, Windham-Myers L, Tringe SG (2015) Patterns in wetland microbial community composition and functional gene repertoire associated with methane emissions. mBio 6(3):e00066–e00015

    CAS  Google Scholar 

  • Ho T, Scranton MI, Taylor GT, Varela R, Thunell RC, Mullerkarger FE (2002) Acetate cycling in the water column of the Cariaco Basin: seasonal and vertical variability and implication for carbon cycling. Limnol Oceanogr 47(4):1119–1128

    Article  CAS  Google Scholar 

  • Holgerson MA, Raymond PA (2016) Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nature Geosci 9:222–226

    Article  CAS  Google Scholar 

  • Huttunen JT, Väisänen TS, Hellsten SK, Heikkinen M, Nykänen H, Jungner H, Niskanen A, Virtanen MO, Lindqvist OV, Nenonen O, Martikainen PJ (2002) Fluxes of CH4, CO2, and N2O in hydroelectric reservoirs Lokka and Porttipahta in the northern boreal zone in Finland. Global Biogeochem Cycles 16. https://doi.org/10.1029/2000GB001316

  • Johansson AE, Gustavsson AM, Öquist MG, Svensson BH (2004) Methane emissions from a constructed wetland treating wastewater-seasonal and spatial distribution and dependence on edaphic factors. Water Res 38:3960–3970

    Article  CAS  Google Scholar 

  • Kankaala P, Taipale S, Nykänen H, Jones RI (2007) Oxidation, efflux, and isotopic fractionation of methane during autumnal turnover in a polyhumic, boreal lake. J Geophys Res 112:G02033. https://doi.org/10.1029/2006JG000336

    Article  CAS  Google Scholar 

  • Klintzsch T, Langer G, Nehrke G, Wieland A, Lenhart K, Keppler F (2019) Methane production by three widespread marine phytoplankton species: release rates, precursor compounds, and potential relevance for the environment. Biogeosciences 16:4129–4144

    Article  CAS  Google Scholar 

  • Knox M, Quay PD, Wilbur D (1992) Kinetic isotopic fractionation during air-water gas transfer of O2, N2, CH4, and H2. J Geophys Res 97:335–343

    Article  Google Scholar 

  • Koelbener A, Ström L, Edwards PJ, Venterink HO (2010) Plant species from mesotrophic wetlands cause relatively high methane emissions from peat soil. Plant Soil 326:147–158

    Article  CAS  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 Microbiol 69:2423–2429

    Article  CAS  Google Scholar 

  • Laanbroek HJ (2010) Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Ann Bot 105(1):141–153

    Article  CAS  Google Scholar 

  • Lee HJ, Jung JY, Oh YK, Lee SS, Madsen EL, Jeon CO (2012) Comparative survey of rumen microbial communities and metabolites across one caprine and three bovine groups, using bar-coded pyro sequencing and 1Hnuclear magnetic resonance spectros copy. Appl Environ Microbiol 78:5983–5993

    Article  CAS  Google Scholar 

  • Lennon JT, Faiia AM, Feng X, Cottingham KL (2006) Relative importance of CO2 recycling and CH4 pathways in lake food webs along a dissolved organic carbon gradient. Limnol Oceanogr 51:1602–1613

    Article  CAS  Google Scholar 

  • Li T, Raivonen M, Alekseychik P, Aurela M, Lohila A, Zheng X, Zhang Q, Wang G, Mammarella I, Rinne J, Yu L, Xie B, Vesala T, Zhang W (2016) Importance of vegetation classes in modeling CH4 emissions from boreal and subarctic wetlands in Finland. Sci Total Environ 572:1111–1122

    Article  CAS  Google Scholar 

  • Liang X, Zhang X, Sun Q, He C, Chen X, Liu X, Chen Z (2016) The role of filamentous algae Spirogyra spp. in methane production and emissions in streams. Aquat Sci 78:227–239

    Article  CAS  Google Scholar 

  • Liang X, Xing T, Li J, Wang B, Wang F, He C, Hou L, Li S (2019) Control of the hydraulic load on nitrous oxide emissions from cascade reservoirs. Environ Sci Technol 53:11745–11754

    Article  CAS  Google Scholar 

  • Lilkanen A, Martikainen PJ (2003) Effect of ammonium and oxygen on methane and nitrous oxide fluxes across sediment-water interface in a eutrophic lake. Chemosphere 52:1287–1293

    Article  CAS  Google Scholar 

  • Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530

    Article  CAS  Google Scholar 

  • Marotta H, Pinho L, Gudasz C, Bastviken D, Tranvik LJ, Enrichprast A (2014) Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nature Clim Change 4:467–470

    Article  CAS  Google Scholar 

  • Martinez D, Anderson MA (2013) Methane production and ebullition in a shallow, artificially aerated, eutrophic temperate lake (Lake Elsinore, CA). Sci Total Environ 454–455:457–465

    Article  CAS  Google Scholar 

  • McDonald IR, Murrell JC (1997) The articulate methane monooxygenase gene pmoA and its use as a functional gene probe for methanotrophs. FEMS Microbiol Lett 156:205–210

    Article  CAS  Google Scholar 

  • McDonald IR, Bodrossy L, Chen Y, Murrell JC (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74:1305–1315

    Article  CAS  Google Scholar 

  • Mcginnis DF, Greinert J, Artemov Y, Beaubien SE, Wuest A (2006) Fate of rising methane bubbles in stratified waters: How much methane reaches the atmosphere? J Geophys Res 111(C09007):1–15. https://doi.org/10.1029/2005JC003183

    Article  CAS  Google Scholar 

  • Megonigal JP, Schlesinger W (2002) Methane-limited methanotrophy in tidal freshwater swamps. Global Biogeochem Cycles 16(4):1088

    Article  CAS  Google Scholar 

  • Messyasz B, Pikosz M, Treska E (2018) Biology of freshwater macroalgae and their distribution. In: Chojnacka K, Wieczorek P, Schroeder G, Michalak I (eds) Algae biomass: characteristics and applications. Developments in Applied Phycology, vol 8. Springer, Cham

    Google Scholar 

  • Nahlik AM, Mitsch WJ (2011) Methane emissions from tropical freshwater wetlands located in different climatic zones of Costa Rica. Glob Change Biol 17:1321–1334

    Article  Google Scholar 

  • Power M, Lowe R, Furey P, Welter J, Limm M, Finlay J, Bode C, Chang S, Goodrich M, Sculley J (2009) Algal mats and insect emergence in rivers under Mediterranean climates: towards photogrammetric surveillance. Freshwater Biol 54:2101–2115

    Article  CAS  Google Scholar 

  • Roussel H, Tenhage L, Joachim S, Cohu R, Gauthier L, Bonzom J (2007) A long-term copper exposure on freshwater ecosystem using lotic mesocosms: primary producer community responses. Aquat Toxicol 81:168–182

    Article  CAS  Google Scholar 

  • Sawakuchi HO, Bastviken D, Sawakuchi AO, Ward ND, Borges CD, Tsai SM, Richey JE, Ballester MVR, Krusche AV (2016) Oxidative mitigation of aquatic methane emissions in large Amazonian rivers. Glob Change Biol 22:1075–1085

    Article  Google Scholar 

  • Schulz S, Conrad R (1995) Effect of algal deposition on acetate and methane concentrations in the profundal sediment of a deep lake (Lake Constance). FEMS Microbiol Ecol 16(4):251–259

    Article  CAS  Google Scholar 

  • Shelley F, Abdullahi F, Grey J, Trimmer M (2015) Microbial methane cycling in the bed of a chalk river: oxidation has the potential to match methanogenesis enhanced by warming. Freshw Biol 60:150–160

    Article  CAS  Google Scholar 

  • Stanley EH, Casson NJ, Christel ST, Crawford JT, Loken LC, Oliver SK (2016) The ecology of methane in streams and rivers: patterns controls, and global significance. Ecol Monogr 86:146–171

    Article  Google Scholar 

  • Stevenson R, Bennett B, Jordan D, French R (2012) Phosphorus regulates stream injury by filamentous green algae, DO, and pH with thresholds in responses. Hydrobiologia 695:25–42

    Article  CAS  Google Scholar 

  • Sun Y, Wen C, Liang X, He C (2018) Determination of the phytoremediation efficiency of Ricinus communis L. and methane uptake from cadmium and nickel-contaminated soil using spent mushroom substrate. Environ Sci Pollut R 25:32603–32616

    Article  CAS  Google Scholar 

  • Tang KW, McGinnis DF, Frindte K, Brüchert V, Grossart HP (2014) Paradox reconsidered: methane oversaturation in well-oxygenated lake waters. Limnol Oceanogr 59:275–284

    Article  Google Scholar 

  • Tremblay AL, Roehm VC, Garneu M (2005) Greenhouse gas emissions-fluxes and processes. Springer Verlag

  • UNESCO/IHA (2010) GHG Measurement Guidelines for Freshwater Reservoirs. UNESCO/IHA, London

    Google Scholar 

  • West WE, Coloso JJ, Jones SE (2012) Effects of algal and terrestrial carbon on methane production rates and methanogen community structure in a temperate lake sediment. Freshw Biol 57:949–955

    Article  CAS  Google Scholar 

  • Wiesenburg DA, Guinasso JNL (1979) Equilibrium solubilities of methane carbon monoxide, hydrogen in water and seawater. J Chem Eng Data 24:356–360

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the kind help of Qiao Sun, Bingbing Li, Wenjing Zhang, and Xuecheng Yang for the fieldwork and the sample analysis. The authors are also grateful to Prof. Mary Power for helpful advice during the preparation of this paper. We also thank the anonymous reviewers and the editors for their insightful comments.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This work was supported by the National Natural Science Foundation of China (41773076 and 41373097).

Author information

Authors and Affiliations

  1. School of Environmental and Chemical Engineering, Shanghai University, Shanghai, 200444, China

    Dan Mei, Ming Ni, Xia Liang, Feifei Wang & Chiquan He

  2. State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai, 200244, China

    Xia Liang & Lijun Hou

Authors
  1. Dan Mei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xia Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lijun Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Feifei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chiquan He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Conceptualization and methodology were proposed by Xia Liang and Lijun Hou. Formal analysis and investigation were performed by Dan Mei and Ming Ni. The original draft was prepared by Dan Mei, Ni Ming, Xia Liang, Feifei Wang, and Chiquan He, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Xia Liang.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Ethics approval and consent to participate

Not applicable.

Consent to Publish

Not applicable.

Additional information

Responsible Editor: Thomas Hein

Publisher’s note

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

Highlights

• Filamentous green algae Spirogyra regulated methane (CH4) emissions from eutrophic rivers.

• High dissolved oxygen during Spirogyra bloom promoted the CH4 consumption by enhancing sediment CH4 oxidation.

• Algal-linked oxic water CH4 production as a major component of water CH4 promoted the CH4 emissions.

Electronic supplementary material

ESM 1

(DOCX 164 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mei, D., Ni, M., Liang, X. et al. Filamentous green algae Spirogyra regulates methane emissions from eutrophic rivers. Environ Sci Pollut Res 28, 3660–3671 (2021). https://doi.org/10.1007/s11356-020-10754-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10754-8

Keywords

Search

Navigation