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Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO2/CH4 Production Ratios.

Abstract

Northern peatlands in general have high methane (CH4) emissions, but individual peatlands show considerable variation as CH4 sources. Particularly in nutrient-poor peatlands, CH4 production can be low and exceeded by carbon dioxide (CO2) production from unresolved anaerobic processes. To clarify the role anaerobic bacterial degraders play in this variation, we compared consumers of cellobiose-derived carbon in two fens differing in nutrient status and the ratio of CO2 to CH4 produced. After [13C]cellobiose amendment, the mesotrophic fen produced equal amounts of CH4 and CO2 The oligotrophic fen had lower CH4 production but produced 3 to 59 times more CO2 than CH4 RNA stable-isotope probing revealed that in the mesotrophic fen with higher CH4 production, cellobiose-derived carbon was mainly assimilated by various recognized fermenters of Firmicutes and by Proteobacteria The oligotrophic peat with excess CO2 production revealed a wider variety of cellobiose-C consumers, including Firmicutes and Proteobacteria, but also more unconventional degraders, such as Telmatobacter-related Acidobacteria and subphylum 3 of Verrucomicrobia Prominent and potentially fermentative Planctomycetes and Chloroflexi did not appear to process cellobiose-C. Our results show that anaerobic degradation resulting in different levels of CH4 production can involve distinct sets of bacterial degraders. By distinguishing cellobiose degraders from the total community, this study contributes to defining anaerobic bacteria that process cellulose-derived carbon in peat. Several of the identified degraders, particularly fermenters and potential Fe(III) or humic substance reducers in the oligotrophic peat, represent promising candidates for resolving the origin of excess CO2 production in peatlands.

IMPORTANCE

Peatlands are major sources of the greenhouse gas methane (CH4), yet in many peatlands, CO2 production from unresolved anaerobic processes exceeds CH4 production. Anaerobic degradation produces the precursors of CH4 production but also represents competing processes. We show that anaerobic degradation leading to high or low CH4 production involved distinct sets of bacteria. Well-known fermenters dominated in a peatland with high CH4 production, while novel and unconventional degraders could be identified in a site where CO2 production greatly exceeds CH4 production. Our results help identify and assign functions to uncharacterized bacteria that promote or inhibit CH4 production and reveal bacteria potentially producing the excess CO2 in acidic peat. This study contributes to understanding the microbiological basis for different levels of CH4 emission from peatlands.

Authors+Show Affiliations

Department of Biosciences, General Microbiology, University of Helsinki, Helsinki, Finland heli.juottonen@alumni.helsinki.fi. Department of Ecology and Genetics, Limnology, Uppsala University, Uppsala, Sweden. Natural Resources Institute Finland, Helsinki, Finland.Department of Ecology and Genetics, Limnology, Uppsala University, Uppsala, Sweden.Department of Environmental and Biological Sciences, University of Eastern Finland, Kuopio, Finland.School of Forest Sciences, University of Eastern Finland, Joensuu, Finland.Department of Biosciences, General Microbiology, University of Helsinki, Helsinki, Finland.Natural Resources Institute Finland, Helsinki, Finland.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27913414

Citation

Juottonen, Heli, et al. "Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens With Different CO2/CH4 Production Ratios." Applied and Environmental Microbiology, vol. 83, no. 4, 2017.
Juottonen H, Eiler A, Biasi C, et al. Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO2/CH4 Production Ratios. Appl Environ Microbiol. 2017;83(4).
Juottonen, H., Eiler, A., Biasi, C., Tuittila, E. S., Yrjälä, K., & Fritze, H. (2017). Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO2/CH4 Production Ratios. Applied and Environmental Microbiology, 83(4), doi:10.1128/AEM.02533-16.
Juottonen H, et al. Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens With Different CO2/CH4 Production Ratios. Appl Environ Microbiol. 2017 02 15;83(4) PubMed PMID: 27913414.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO2/CH4 Production Ratios. AU - Juottonen,Heli, AU - Eiler,Alexander, AU - Biasi,Christina, AU - Tuittila,Eeva-Stiina, AU - Yrjälä,Kim, AU - Fritze,Hannu, Y1 - 2017/02/01/ PY - 2016/09/02/received PY - 2016/11/28/accepted PY - 2016/12/4/pubmed PY - 2017/11/29/medline PY - 2016/12/4/entrez KW - anaerobic degradation KW - greenhouse gas KW - methane KW - microbial communities KW - peat KW - stable-isotope probing KW - wetland JF - Applied and environmental microbiology JO - Appl. Environ. Microbiol. VL - 83 IS - 4 N2 - : Northern peatlands in general have high methane (CH4) emissions, but individual peatlands show considerable variation as CH4 sources. Particularly in nutrient-poor peatlands, CH4 production can be low and exceeded by carbon dioxide (CO2) production from unresolved anaerobic processes. To clarify the role anaerobic bacterial degraders play in this variation, we compared consumers of cellobiose-derived carbon in two fens differing in nutrient status and the ratio of CO2 to CH4 produced. After [13C]cellobiose amendment, the mesotrophic fen produced equal amounts of CH4 and CO2 The oligotrophic fen had lower CH4 production but produced 3 to 59 times more CO2 than CH4 RNA stable-isotope probing revealed that in the mesotrophic fen with higher CH4 production, cellobiose-derived carbon was mainly assimilated by various recognized fermenters of Firmicutes and by Proteobacteria The oligotrophic peat with excess CO2 production revealed a wider variety of cellobiose-C consumers, including Firmicutes and Proteobacteria, but also more unconventional degraders, such as Telmatobacter-related Acidobacteria and subphylum 3 of Verrucomicrobia Prominent and potentially fermentative Planctomycetes and Chloroflexi did not appear to process cellobiose-C. Our results show that anaerobic degradation resulting in different levels of CH4 production can involve distinct sets of bacterial degraders. By distinguishing cellobiose degraders from the total community, this study contributes to defining anaerobic bacteria that process cellulose-derived carbon in peat. Several of the identified degraders, particularly fermenters and potential Fe(III) or humic substance reducers in the oligotrophic peat, represent promising candidates for resolving the origin of excess CO2 production in peatlands. IMPORTANCE: Peatlands are major sources of the greenhouse gas methane (CH4), yet in many peatlands, CO2 production from unresolved anaerobic processes exceeds CH4 production. Anaerobic degradation produces the precursors of CH4 production but also represents competing processes. We show that anaerobic degradation leading to high or low CH4 production involved distinct sets of bacteria. Well-known fermenters dominated in a peatland with high CH4 production, while novel and unconventional degraders could be identified in a site where CO2 production greatly exceeds CH4 production. Our results help identify and assign functions to uncharacterized bacteria that promote or inhibit CH4 production and reveal bacteria potentially producing the excess CO2 in acidic peat. This study contributes to understanding the microbiological basis for different levels of CH4 emission from peatlands. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/27913414/Distinct_Anaerobic_Bacterial_Consumers_of_Cellobiose_Derived_Carbon_in_Boreal_Fens_with_Different_CO2/CH4_Production_Ratios_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=27913414 DB - PRIME DP - Unbound Medicine ER -