Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO ₂ /CH ₄ Production Ratios

Abstract

Northern peatlands in general have high methane (CH 4 ) emissions, but individual peatlands show considerable variation as CH 4 sources. Particularly in nutrient-poor peatlands, CH 4 production can be low and exceeded by carbon dioxide (CO 2 ) 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 CO 2 to CH 4 produced. After [ 13 C]cellobiose amendment, the mesotrophic fen produced equal amounts of CH 4 and CO 2 . The oligotrophic fen had lower CH 4 production but produced 3 to 59 times more CO 2 than CH 4 . RNA stable-isotope probing revealed that in the mesotrophic fen with higher CH 4 production, cellobiose-derived carbon was mainly assimilated by various recognized fermenters of Firmicutes and by Proteobacteria. The oligotrophic peat with excess CO 2 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 CH 4 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 CO 2 production in peatlands.IMPORTANCE Peatlands are major sources of the greenhouse gas methane (CH 4 ), yet in many peatlands, CO 2 production from unresolved anaerobic processes exceeds CH 4 production. Anaerobic degradation produces the precursors of CH 4 production but also represents competing processes. We show that anaerobic degradation leading to high or low CH 4 production involved distinct sets of bacteria. Well-known fermenters dominated in a peatland with high CH 4 production, while novel and unconventional degraders could be identified in a site where CO 2 production greatly exceeds CH 4 production. Our results help identify and assign functions to uncharacterized bacteria that promote or inhibit CH 4 production and reveal bacteria potentially producing the excess CO 2 in acidic peat. This study contributes to understanding the microbiological basis for different levels of CH 4 emission from peatlands.

Soil viruses are underexplored players in ecosystem carbon processing

“…SDB, another acidophilic chemoorganoheterotroph, but an obligate anaerobe, with a known syntrophic relationship with methanogens (94, 95). Collectively, these virus-host linkages provide evidence for the Mire’s viruses to be impacting the C cycle via population control of relevant C-cycling hosts, consistent with previous results in this system (46) and other wetlands (96).…”

Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing

“…strain SDB, another acidophilic chemoorganoheterotroph but an obligate anaerobe, with a known syntrophic relationship with methanogens ( 97 , 98 ). Collectively, these virus-host linkages provide evidence for the Mire’s viruses to be impacting the C cycle via population control of relevant C-cycling hosts, consistent with previous results in this system ( 46 ) and other wetlands ( 99 ).…”

Rare Species Shift the Structure of Bacterial Communities Across Sphagnum Compartments in a Subalpine Peatland

“…Among keystone species, Candidatus Nitrotoga are cold-adapted nitrite-oxidizing bacteria, which involved in nitrogen cycling (Alawi et al, 2007). Spirochaeta are anaerobic bacteria, and some members are capable of cellulose-derivative degradation (glucose and cellobiose) and methane production in peat soils (Schmidt et al, 2015;Juottonen et al, 2017). These keystone species may benefit Sphagnum development under extreme conditions and FIGURE 3 | Composition of bacterial communities in WBC (A), AT (B), RT (C), and CART (D).…”