Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland

X, Lin; Green, Stefan J.; Tfaily, Malak M.; Prakash, Om; Konstantinidis, Konstantinos T.; Corbett, J. E.; Chanton, Jeffrey P.; Cooper, William T.; Kostka, Joel E.

doi:10.1128/aem.01750-12

Cited by 146 publications

(113 citation statements)

References 75 publications

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“…Acidobacteria are common in anoxic peat and more prominent with lower pH and oligotrophy (4,33,34,(56)(57)(58)(59). Accordingly, they were more prominent in processing cellobiose-C in the oligotrophic peat than in the mesotrophic peat.…”

Section: Discussionmentioning

confidence: 97%

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

Juottonen

Eiler

Biasi

et al. 2017

Appl Environ Microbiol

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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.

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Section: Discussionmentioning

confidence: 97%

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

Juottonen

Eiler

Biasi

et al. 2017

Appl Environ Microbiol

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“…In general, fewer studies of fungal community composition have been conducted in peatlands using cultivation-independent molecular techniques (19,23). In this study, fungal communities were characterized by high horizontal variation, an increasing proportion of yeast (Saccharomyces), and a reduction of the whiterot fungi (Agaricomycotina) with depth.…”

Section: Discussionmentioning

confidence: 99%

“…PCR amplification of bacterial and archaeal small-subunit (SSU) rRNA genes and fungal internal transcribed spacer (ITS) regions of rRNA genes was performed using the primer pairs 515F/806R (35) and ITS1F/ITS4 (36), respectively. Quantitative real-time PCR (qPCR) was performed with 1/40-diluted genomic DNA as the templates to quantify the abundance of total bacterial, archaeal, and fungal SSU rRNA genes according to the procedures described elsewhere (23,37).…”

Section: Methodsmentioning

confidence: 99%

“…To date, few next-generation-sequencing-based studies have characterized the overall diversity and environmental controls of community dynamics in northern peatlands (17,19). Studies of microbial communities in peat soils have been conducted over relatively small scales, limited to few samples, and often with molecular approaches lacking in phylogenetic resolution or a consideration of spatial and temporal variation (6,(21)(22)(23)(24). In particular, microbial communities in the anoxic, deep peat layers (catotelm) have been largely ignored and the mechanism of microbially mediated carbon turnover in deep peat is relatively unknown (25)(26)(27).…”

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confidence: 99%

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Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA

Tfaily

Steinweg

et al. 2014

Appl Environ Microbiol

109

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e This study investigated the abundance, distribution, and composition of microbial communities at the watershed scale in a boreal peatland within the Marcell Experimental Forest (MEF), Minnesota, USA. Through a close coupling of next-generation sequencing, biogeochemistry, and advanced analytical chemistry, a biogeochemical hot spot was revealed in the mesotelm (30-to 50-cm depth) as a pronounced shift in microbial community composition in parallel with elevated peat decomposition. The relative abundance of Acidobacteria and the Syntrophobacteraceae, including known hydrocarbon-utilizing genera, was positively correlated with carbohydrate and organic acid content, showing a maximum in the mesotelm. The abundance of Archaea (primarily crenarchaeal groups 1.1c and 1.3) increased with depth, reaching up to 60% of total small-subunit (SSU) rRNA gene sequences in the deep peat below the 75-cm depth. Stable isotope geochemistry and potential rates of methane production paralleled vertical changes in methanogen community composition to indicate a predominance of acetoclastic methanogenesis mediated by the Methanosarcinales in the mesotelm, while hydrogen-utilizing methanogens predominated in the deeper catotelm. RNA-derived pyrosequence libraries corroborated DNA sequence data to indicate that the above-mentioned microbial groups are metabolically active in the mid-depth zone. Fungi showed a maximum in rRNA gene abundance above the 30-cm depth, which comprised only an average of 0.1% of total bacterial and archaeal rRNA gene abundance, indicating prokaryotic dominance. Ratios of C to P enzyme activities approached 0.5 at the acrotelm and catotelm, indicating phosphorus limitation. In contrast, P limitation pressure appeared to be relieved in the mesotelm, likely due to P solubilization by microbial production of organic acids and C-P lyases. Based on path analysis and the modeling of community spatial turnover, we hypothesize that P limitation outweighs N limitation at MEF, and microbial communities are structured by the dominant shrub, Chamaedaphne calyculata, which may act as a carbon source for major consumers in the peatland.

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“…The ISME Journal (2015Journal ( ) 9, 2740Journal ( -2744doi:10.1038/ismej.2015published online 22 May 2015 Peatlands represent carbon rich environments shown to sequester approximately one-third of all soil carbon on Earth (Gorham, 1991). Archaea are particularly abundant in peat soils, with Crenarchaea and Thaumarchaeota comprising up to 60% of the microbial community in subsurface peats (Kemnitz et al, 2007;Lin et al, 2012;Basiliko et al, 2013;Hawkins et al, 2014;Lin et al, 2014). Thaumarchaeotal groups 1.1b and 1.1c were recently estimated to account for 76 ± 33% of total archaea in global soil samples (Auguet et al, 2010), suggesting they may have key roles in Earth's biogeochemical cycles.…”

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confidence: 99%

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

Handley

Gilbert

et al. 2015

The ISME Journal

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To probe the metabolic potential of abundant Archaea in boreal peats, we reconstructed two nearcomplete archaeal genomes, affiliated with Thaumarchaeota group 1.1c (bin Fn1, 8% abundance), which was a genomically unrepresented group, and Thermoplasmata (bin Bg1, 26% abundance), from metagenomic data acquired from deep anoxic peat layers. Each of the near-complete genomes encodes the potential to degrade long-chain fatty acids (LCFA) via β-oxidation. Fn1 has the potential to oxidize LCFA either by syntrophic interaction with methanogens or by coupling oxidation with anaerobic respiration using fumarate as a terminal electron acceptor (TEA). Fn1 is the first Thaumarchaeota genome without an identifiable carbon fixation pathway, indicating that this mesophilic phylum encompasses more diverse metabolisms than previously thought. Furthermore, we report genetic evidence suggestive of sulfite and/or organosulfonate reduction by Thermoplasmata Bg1. In deep peat, inorganic TEAs are often depleted to extremely low levels, yet the anaerobic respiration predicted for two abundant archaeal members suggests organic electron acceptors such as fumarate and organosulfonate (enriched in humic substances) may be important for respiration and C mineralization in peatlands.

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Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland

Cited by 146 publications

References 75 publications

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

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

Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

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Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland

Cited by 146 publications

References 75 publications

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

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

Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

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Product

Resources

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

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