scholarly journals Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions

2008 ◽  
Vol 5 (6) ◽  
pp. 1587-1599 ◽  
Author(s):  
B. Orcutt ◽  
C. Meile

Abstract. Anaerobic oxidation of methane (AOM) is the main process responsible for the removal of methane generated in Earth's marine subsurface environments. However, the biochemical mechanism of AOM remains elusive. By explicitly resolving the observed spatial arrangement of methanotrophic archaea and sulfate reducing bacteria found in consortia mediating AOM, potential intermediates involved in the electron transfer between the methane oxidizing and sulfate reducing partners were investigated via a consortium-scale reaction transport model that integrates the effect of diffusional transport with thermodynamic and kinetic controls on microbial activity. Model simulations were used to assess the impact of poorly constrained microbial characteristics such as minimum energy requirements to sustain metabolism and cell specific rates. The role of environmental conditions such as the influence of methane levels on the feasibility of H2, formate and acetate as intermediate species, and the impact of the abundance of intermediate species on pathway reversal were examined. The results show that higher production rates of intermediates via AOM lead to increased diffusive fluxes from the methane oxidizing archaea to sulfate reducing bacteria, but the build-up of the exchangeable species can cause the energy yield of AOM to drop below that required for ATP production. Comparison to data from laboratory experiments shows that under the experimental conditions of Nauhaus et al. (2007), none of the potential intermediates considered here is able to support metabolic activity matching the measured rates.

2008 ◽  
Vol 5 (3) ◽  
pp. 1933-1967 ◽  
Author(s):  
B. Orcutt ◽  
C. Meile

Abstract. Anaerobic oxidation of methane (AOM) is the main process responsible for the removal of methane generated in Earth's marine subsurface environments. However, the biochemical mechanism of AOM remains elusive. By explicitly resolving the observed spatial arrangement of methanotrophic archaea and sulfate reducing bacteria found in consortia mediating AOM, potential intermediates involved in the electron transfer between the methane oxidizing and sulfate reducing partners were investigated via a consortium-scale reaction transport model that integrates the effect of diffusional transport with thermodynamic and kinetic controls on microbial activity. Model simulations were used to assess the impact of poorly constrained microbial characteristics such as minimum energy requirements to sustain metabolism, substrate affinity and cell specific rates. The role of environmental conditions such as the influence of methane levels on the feasibility of H2, formate and acetate as intermediate species, and the impact of the abundance of intermediate species on pathway reversal was examined. The results show that higher production rates of intermediates via AOM lead to increased diffusive fluxes from the methane oxidizing archaea to sulfate reducing bacteria, but the build-up of the exchangeable species causes the energy yield of AOM to drop below that required for ATP production. Comparison to data from laboratory experiments shows that under the experimental conditions of Nauhaus et al. (2007), neither hydrogen nor formate is exchanged fast enough between the consortia partners to achieve measured rates of metabolic activity, but that acetate exchange might support rates that approach those observed.


2001 ◽  
Vol 67 (4) ◽  
pp. 1922-1934 ◽  
Author(s):  
V. J. Orphan ◽  
K.-U. Hinrichs ◽  
W. Ussler ◽  
C. K. Paull ◽  
L. T. Taylor ◽  
...  

ABSTRACT The oxidation of methane in anoxic marine sediments is thought to be mediated by a consortium of methane-consuming archaea and sulfate-reducing bacteria. In this study, we compared results of rRNA gene (rDNA) surveys and lipid analyses of archaea and bacteria associated with methane seep sediments from several different sites on the Californian continental margin. Two distinct archaeal lineages (ANME-1 and ANME-2), peripherally related to the orderMethanosarcinales, were consistently associated with methane seep marine sediments. The same sediments contained abundant13C-depleted archaeal lipids, indicating that one or both of these archaeal groups are members of anaerobic methane-oxidizing consortia. 13C-depleted lipids and the signature 16S rDNAs for these archaeal groups were absent in nearby control sediments. Concurrent surveys of bacterial rDNAs revealed a predominance of δ-proteobacteria, in particular, close relatives ofDesulfosarcina variabilis. Biomarker analyses of the same sediments showed bacterial fatty acids with strong 13C depletion that are likely products of these sulfate-reducing bacteria. Consistent with these observations, whole-cell fluorescent in situ hybridization revealed aggregations of ANME-2 archaea and sulfate-reducing Desulfosarcina andDesulfococcus species. Additionally, the presence of abundant 13C-depleted ether lipids, presumed to be of bacterial origin but unrelated to ether lipids of members of the orderDesulfosarcinales, suggests the participation of additional bacterial groups in the methane-oxidizing process. Although theDesulfosarcinales and ANME-2 consortia appear to participate in the anaerobic oxidation of methane in marine sediments, our data suggest that other bacteria and archaea are also involved in methane oxidation in these environments.


2012 ◽  
Vol 9 (3) ◽  
pp. 1033-1040 ◽  
Author(s):  
M. Barlett ◽  
K. Zhuang ◽  
R. Mahadevan ◽  
D. Lovley

Abstract. Enhancing microbial U(VI) reduction with the addition of organic electron donors is a promising strategy for immobilizing uranium in contaminated groundwaters, but has yet to be optimized because of a poor understanding of the factors controlling the growth of various microbial communities during bioremediation. In previous field trials in which acetate was added to the subsurface, there were two distinct phases: an initial phase in which acetate-oxidizing, U(VI)-reducing Geobacter predominated and U(VI) was effectively reduced and a second phase in which acetate-oxidizing sulfate reducing bacteria (SRB) predominated and U(VI) reduction was poor. The interaction of Geobacter and SRB was investigated both in sediment incubations that mimicked in situ bioremediation and with in silico metabolic modeling. In sediment incubations, Geobacter grew quickly but then declined in numbers as the microbially reducible Fe(III) was depleted whereas the SRB grow more slowly and reached dominance after 30–40 days. Modeling predicted a similar outcome. Additional modeling in which the relative initial percentages of the Geobacter and SRB were varied indicated that there was little to no competitive interaction between Geobacter and SRB when acetate was abundant. Further simulations suggested that the addition of Fe(III) would revive the Geobacter, but have little to no effect on the SRB. This result was confirmed experimentally. The results demonstrate that it is possible to predict the impact of amendments on important components of the subsurface microbial community during groundwater bioremediation. The finding that Fe(III) availability, rather than competition with SRB, is the key factor limiting the activity of Geobacter during in situ uranium bioremediation will aid in the design of improved uranium bioremediation strategies.


2021 ◽  
Author(s):  
Grayson L Chadwick ◽  
Connor T Skennerton ◽  
Rafael Laso-Perez ◽  
Andy O Leu ◽  
Daan R Speth ◽  
...  

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features which separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well-distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.


2018 ◽  
Author(s):  
C. Cassarini ◽  
Y. Zhang ◽  
P. N. Lens

AbstractAnaerobic oxidation of methane (AOM) coupled to sulfate reduction is mediated by, respectively, anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB). When a microbial community from coastal marine Lake Grevelingen sediment, containing ANME-3 as the most abundant type of ANME, was incubated under a pressure gradient (0.1-40 MPa) for 77 days, ANME-3 was more pressure sensitive than the SRB. ANME-3 activity was higher at lower (0.1, 0.45 MPa) over higher (10, 20 and 40 MPa) CH4total pressures. Moreover, the sulfur metabolism was shifted upon changing the incubation pressure: only at 0.1 MPa elemental sulfur was detected in a considerable amount and SRB of theDesulfobacteralesorder were more enriched at elevated pressures than theDesulfubulbaceae. This study provides evidence that ANME-3 can be constrained at shallow environments, despite the scarce bioavailable energy, because of its pressure sensitivity. Besides, the association between ANME-3 and SRB can be steered by changing solely the incubation pressure.ImportanceAnaerobic oxidation of methane (AOM) coupled to sulfate reduction is a biological process largely occurring in marine sediments, which contributes to the removal of almost 90% of sedimentary methane, thereby controlling methane emission to the atmosphere. AOM is mediated by slow growing archaea, anaerobic methanotrophs (ANME) and sulfate reducing bacteria. The enrichment of these microorganisms has been challenging, especially considering the low solubility of methane at ambient temperature and pressure. Previous studies showed strong positive correlations between the growth of ANME and the methane pressure, since the higher the pressure the more methane is dissolved. In this research, a shallow marine sediment was incubated under methane pressure gradients. The investigated effect of pressure on the AOM-SR activity, the formation sulfur intermediates and the microbial community structure is important to understand the pressure influence on the processes and the activity of the microorganisms involved to further understand their metabolism and physiology.


2021 ◽  
Author(s):  
Maria De La Fuente ◽  
Sandra Arndt ◽  
Tim Minshul ◽  
Héctor Marín-Moreno

<p>Large quantities of methane (CH<sub>4</sub>) are stored in gas hydrates at shallow depths within marine sediments. These reservoirs are highly sensitive to ocean warming and if destabilized could lead to significant CH<sub>4</sub> release and global environmental impacts. However, the existence of such a positive feedback loop has recently been questioned as efficient CH<sub>4 </sub>sinks within the sediment-ocean continuum likely mitigate the impact of gas hydrate-derived CH<sub>4</sub> emissions on global climate. In particular, benthic anaerobic oxidation of methane (AOM) represents an important CH<sub>4 </sub>sink capable of completely consuming CH<sub>4</sub> fluxes before they reach the seafloor. However, the efficiency of this benthic biofilter is controlled by a complex interplay of multiphase methane transport and microbial oxidation processes and is thus highly variable (0-100%). In addition, AOM potentially enhances benthic alkalinity fluxes with important, yet largely overlooked implications for ocean pH, saturation state and CO<sub>2</sub> emissions. As a consequence, the full environmental impact of hydrate-derived CH<sub>4</sub> release to the ocean-atmosphere system and its feedbacks on global biogeochemical cycles and climate still remain poorly quantified. To the best our knowledge, currently available modelling tools to assess the benthic CH<sub>4</sub> sink and its environmental impact during hydrate dissociation do not account for the full complexity of the problem. Available codes generally do not explicitly resolve the dynamics of the microbial community and thus fail to represent transient changes in AOM biofilter efficiency and windows of opportunity for CH<sub>4</sub> escape. They also highly simplify the representation of  multiphase CH<sub>4 </sub>transport processes and gas hydrate dynamics and rarely assess the influence of hydrate-derived CH<sub>4</sub> fluxes on benthic-pelagic alkalinity and dissolved inorganic carbon fluxes. To overcome these limitations, we have developed a novel 1D thermo-hydro-biogeochemical hydrate model that improve the quantitative understanding of the benthic CH<sub>4</sub> sink and benthic carbon cycle-climate feedbacks in response to methane hydrate dissociation caused by temperature and sea-level perturbations. Our mathematical model builds on previous thermo-hydraulic hydrate simulators, expanding them to include the dominant microbial processes affecting CH<sub>4</sub> fluxes in a consistent and coupled mathematical formulation. The micro-biogeochemical reaction network accounts for the main redox reactions (i.e., aerobic degradation, organoclastic sulphate reduction (OSR), methanogenesis and aerobic-anaerobic oxidation of methane (AeOM-AOM)), carbonate dissolution/precipitation and equilibrium reactions that drive biogeochemical dynamics in marine hydrate-bearing sediments . In particular, the AOM rate is expressed as a bioenergetic rate law that explicitly accounts for biomass dynamics. Finally, the model allows tracking the carbon isotope signatures of all dissolved and solid carbon species. In this talk we will present the model structure for the multiphase-multicomponent hydrate system, describe the specific constitutive and reaction equations used in the formulation, discuss the numerical strategy implemented and illustrate the potential capabilities of the model.</p>


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