Competing Formate- and Carbon Dioxide-Utilizing Prokaryotes in an Anoxic Methane-Emitting Fen Soil

Hunger, Sindy; Schmidt, Oliver; Hilgarth, Maik; Horn, Marcus A.; Kolb, Steffen; Conrad, Ralf; Drake, Harold L.

doi:10.1128/aem.00282-11

Cited by 62 publications

(61 citation statements)

References 86 publications

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“…Methanogens and acetogens commonly have neutral pH optima as they rely on a membrane proton gradient for energy conservation (Whitman et al,, 2001;Drake et al, 2013) and therefore must be well adapted, that is, buffered intracellularly, to survive in these environments. Their ecological importance for the flow of carbon and reductants was shown for other acidic environments (Horn et al, 2003;Cadillo-Quiroz et al, 2006;Drake et al, 2009;Hunger et al, 2011), and their Figure 6 Conceptual model of carbon flow from volcanic CO 2 to soil carbon in the mofette summarizing the observed effects of extreme CO 2 degassing on a wetland soil. Promoted CO 2 utilization and key microbial taxa are presented.…”

Section: Bacterial Groups Assimilating Volcanic Comentioning

confidence: 99%

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

et al. 2014

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Effects of extremely high carbon dioxide (CO 2 ) concentrations on soil microbial communities and associated processes are largely unknown. We studied a wetland area affected by spots of subcrustal CO 2 degassing (mofettes) with focus on anaerobic autotrophic methanogenesis and acetogenesis because the pore gas phase was largely hypoxic. Compared with a reference soil, the mofette was more acidic (DpH B0.8), strongly enriched in organic carbon (up to 10 times), and exhibited lower prokaryotic diversity. It was dominated by methanogens and subdivision 1 Acidobacteria, which likely thrived under stable hypoxia and acidic pH. Anoxic incubations revealed enhanced formation of acetate and methane (CH 4 ) from hydrogen (H 2 ) and CO 2 consistent with elevated CH 4 and acetate levels in the mofette soil. 13 CO 2 mofette soil incubations showed high label incorporations with B512 ng 13 C g (dry weight (dw)) soil À 1 d À 1 into the bulk soil and up to 10.7 ng 13 C g (dw) soil À 1 d À 1 into almost all analyzed bacterial lipids. Incorporation of CO 2 -derived carbon into archaeal lipids was much lower and restricted to the first 10 cm of the soil. DNA-SIP analysis revealed that acidophilic methanogens affiliated with Methanoregulaceae and hitherto unknown acetogens appeared to be involved in the chemolithoautotrophic utilization of 13 CO 2 . Subdivision 1 Acidobacteriaceae assimilated 13 CO 2 likely via anaplerotic reactions because Acidobacteriaceae are not known to harbor enzymatic pathways for autotrophic CO 2 assimilation. We conclude that CO 2 -induced geochemical changes promoted anaerobic and acidophilic organisms and altered carbon turnover in affected soils.

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Section: Bacterial Groups Assimilating Volcanic Comentioning

confidence: 99%

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

et al. 2014

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“…A conservative threshold value of 87.5% was used for determining family-level OTUs of 16S rRNA gene sequences (Yarza et al, 2008). A conservative threshold value of 85.7% was used for creating species-level OTUs of mcrA and mrtA sequences (Hunger et al, 2011); a maximal identity of p85.7% is indicated by 'spp.' after the genus name.…”

Section: Sequence Analysesmentioning

confidence: 99%

Methanogenic food web in the gut contents of methane-emitting earthwormEudrilus eugeniaefrom Brazil

et al. 2015

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The anoxic saccharide-rich conditions of the earthworm gut provide an ideal transient habitat for ingested microbes capable of anaerobiosis. It was recently discovered that the earthworm Eudrilus eugeniae from Brazil can emit methane (CH 4 ) and that ingested methanogens might be associated with this emission. The objective of this study was to resolve trophic interactions of bacteria and methanogens in the methanogenic food web in the gut contents of E. eugeniae. RNA-based stable isotope probing of bacterial 16S rRNA as well as mcrA and mrtA (the alpha subunit of methyl-CoM reductase and its isoenzyme, respectively) of methanogens was performed with [ 13 C]-glucose as a model saccharide in the gut contents. Concomitant fermentations were augmented by the rapid consumption of glucose, yielding numerous products, including molecular hydrogen (H 2 ), carbon dioxide (CO 2 ), formate, acetate, ethanol, lactate, succinate and propionate. Aeromonadaceaeaffiliated facultative aerobes, and obligate anaerobes affiliated to Lachnospiraceae, Veillonellaceae and Ruminococcaceae were associated with the diverse fermentations. Methanogenesis was ongoing during incubations, and 13 C-labeling of CH 4 verified that supplemental [ 13 C]-glucose derived carbon was dissimilated to CH 4 . Hydrogenotrophic methanogens affiliated with Methanobacteriaceae and Methanoregulaceae were linked to methanogenesis, and acetogens related to Peptostreptoccocaceae were likewise found to be participants in the methanogenic food web. H 2 rather than acetate stimulated methanogenesis in the methanogenic gut content enrichments, and acetogens appeared to dissimilate supplemental H 2 to acetate in methanogenic enrichments. These findings provide insight on the processes and associated taxa potentially linked to methanogenesis and the turnover of organic carbon in the alimentary canal of methane-emitting E. eugeniae.

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“…Thus, the fractionation factor for total acetate (ε acetate total ϭ Ϫ57.3‰ Ϯ 2.3‰) was similar to that of the methyl group of acetate (ε methyl ϭ Ϫ58.2‰ Ϯ 3.1‰). These data have frequently been used to interpret environmental isotopic signatures of acetate in, for example, lake sediments (14-19), rice paddies (20-23), and marine environments (24-27).However, this reported value may not cover all acetogens, since they are metabolically, ecologically, and phylogenetically diverse (25,(28)(29)(30). We know from different methanogenic archaea, which likewise utilize the acetyl-CoA pathway to produce CH 4 from H 2 and CO 2 , that the fractionation factors range from Ϫ25‰ (31) to Ϫ69‰ (32; reviewed in reference 9).…”

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confidence: 99%

“…However, this reported value may not cover all acetogens, since they are metabolically, ecologically, and phylogenetically diverse (25,(28)(29)(30). We know from different methanogenic archaea, which likewise utilize the acetyl-CoA pathway to produce CH 4 from H 2 and CO 2 , that the fractionation factors range from Ϫ25‰ (31) to Ϫ69‰ (32; reviewed in reference 9).…”

mentioning

confidence: 99%

Carbon Isotope Fractionation of 11 Acetogenic Strains Grown on H ₂ and CO ₂

Blaser

Dreisbach

Conrad

2013

Appl Environ Microbiol

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Acetogenic bacteria are able to grow autotrophically on hydrogen and carbon dioxide by using the acetyl coenzyme A (acetyl-CoA) pathway. Acetate is the end product of this reaction. In contrast to the fermentative route of acetate production, which shows almost no fractionation of carbon isotopes, the acetyl-CoA pathway has been reported to exhibit a preference for light carbon. In Acetobacterium woodii the isotope fractionation factor () for 13 C and 12 C has previously been reported to be ‫؍‬ ؊58.6‰. To investigate whether such a strong fractionation is a general feature of acetogenic bacteria, we measured the stable carbon isotope fractionation factor of 10 acetogenic strains grown on H 2 and CO 2 . The average fractionation factor was TIC ‫؍‬ ؊57.2‰ for utilization of total inorganic carbon and acetate ‫؍‬ ؊54.6‰ for the production of acetate. The strongest fractionation was found for Sporomusa sphaeroides ( TIC ‫؍‬ ؊68.3‰), the lowest fractionation for Morella thermoacetica ( TIC ‫؍‬ ؊38.2‰). To investigate the reproducibility of our measurements, we determined the fractionation factor of 21 biological replicates of Thermoanaerobacter kivui. In general, our study confirmed the strong fractionation of stable carbon during chemolithotrophic acetate formation in acetogenic bacteria. However, the specific characteristics of the bacterial strain, as well as the cultural conditions, may have a moderate influence on the overall fractionation.A cetate is a central intermediate in the anaerobic degradation of organic matter and originates either from fermentation of organic compounds or from reduction of CO 2 with H 2 via the acetyl coenzyme A (acetyl-CoA) pathway (acetogenesis). The produced acetate serves as an important substrate for other microbes, e.g., for acetoclastic methanogens. The pathways involved in acetate turnover can be differentiated if the fractionation factors (ε) of the individual processes (e.g., fermentation, acetogenesis, and methanogenesis) are known (1). The fractionation factor can be quantified from the natural abundance of 13 C in acetate, organic carbon, inorganic carbon, and methane, which can all be measured in environmental samples.In anoxic environments and pure cultures of anaerobic microorganisms mainly the acetate degradation processes (methanogenesis and sulfate or sulfur reduction) have been investigated for the isotopic fractionation factors (2-10). The production of acetate, however, is less well characterized. In general it has been reported that fermentation exhibits only a weak (Ͻ5‰) fractionation (11-13). On the other hand, acetate production via chemolithotrophic acetogenesis fractionates stronger. However, it has thus far only been studied in Acetobacterium woodii (2). There a mean fractionation factor of ε ϭ Ϫ58.6‰ Ϯ 0.7‰ was reported, with both branches of the acetyl-CoA pathway contributing equally. Thus, the fractionation factor for total acetate (ε acetate total ϭ Ϫ57.3‰ Ϯ 2.3‰) was similar to that of the methyl group of acetate (ε methyl ϭ Ϫ58.2‰ Ϯ 3.1‰). These dat...

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Competing Formate- and Carbon Dioxide-Utilizing Prokaryotes in an Anoxic Methane-Emitting Fen Soil

Cited by 62 publications

References 86 publications

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

Methanogenic food web in the gut contents of methane-emitting earthwormEudrilus eugeniaefrom Brazil

Carbon Isotope Fractionation of 11 Acetogenic Strains Grown on H ₂ and CO ₂

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Competing Formate- and Carbon Dioxide-Utilizing Prokaryotes in an Anoxic Methane-Emitting Fen Soil

Cited by 62 publications

References 86 publications

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette

Methanogenic food web in the gut contents of methane-emitting earthwormEudrilus eugeniaefrom Brazil

Carbon Isotope Fractionation of 11 Acetogenic Strains Grown on H 2 and CO 2

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Carbon Isotope Fractionation of 11 Acetogenic Strains Grown on H ₂ and CO ₂