scholarly journals Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea

mBio ◽  
2017 ◽  
Vol 8 (4) ◽  
Author(s):  
Connor T. Skennerton ◽  
Karuna Chourey ◽  
Ramsunder Iyer ◽  
Robert L. Hettich ◽  
Gene W. Tyson ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Direct Electron Transfer ◽  
Sulfate Reducing Bacteria ◽  
Recent Analysis ◽  
Extracellular Electron Transfer ◽  
Multiple Partner ◽  
Sulfate Reducing ◽  
Primary Mechanism ◽  
Anaerobic Methanotrophs ◽  
Reducing Bacteria

ABSTRACT The anaerobic oxidation of methane by anaerobic methanotrophic (ANME) archaea in syntrophic partnership with deltaproteobacterial sulfate-reducing bacteria (SRB) is the primary mechanism for methane removal in ocean sediments. The mechanism of their syntrophy has been the subject of much research as traditional intermediate compounds, such as hydrogen and formate, failed to decouple the partners. Recent findings have indicated the potential for extracellular electron transfer from ANME archaea to SRB, though it is unclear how extracellular electrons are integrated into the metabolism of the SRB partner. We used metagenomics to reconstruct eight genomes from the globally distributed SEEP-SRB1 clade of ANME partner bacteria to determine what genomic features are required for syntrophy. The SEEP-SRB1 genomes contain large multiheme cytochromes that were not found in previously described free-living SRB and also lack periplasmic hydrogenases that may prevent an independent lifestyle without an extracellular source of electrons from ANME archaea. Metaproteomics revealed the expression of these cytochromes at in situ methane seep sediments from three sites along the Pacific coast of the United States. Phylogenetic analysis showed that these cytochromes appear to have been horizontally transferred from metal-respiring members of the Deltaproteobacteria such as Geobacter and may allow these syntrophic SRB to accept extracellular electrons in place of other chemical/organic electron donors. IMPORTANCE Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria. IMPORTANCE Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.

scholarly journals Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor

2005 ◽  
Vol 71 (7) ◽  
pp. 3725-3733 ◽  
Author(s):  
Peter R. Girguis ◽  
Aaron E. Cozen ◽  
Edward F. DeLong
Keyword(s):  
Bacterial Growth ◽  
Growth Rates ◽  
Continuous Flow ◽  
Flow Regimes ◽  
Sulfate Reducing Bacteria ◽  
Flow Rates ◽  
Sulfate Reducing ◽  
Oxidation Rates ◽  
Anaerobic Methanotrophs ◽  
Reducing Bacteria

ABSTRACT The consumption of methane in anoxic marine sediments is a biogeochemical phenomenon mediated by two archaeal groups (ANME-1 and ANME-2) that exist syntrophically with sulfate-reducing bacteria. These anaerobic methanotrophs have yet to be recovered in pure culture, and key aspects of their ecology and physiology remain poorly understood. To characterize the growth and physiology of these anaerobic methanotrophs and the syntrophic sulfate-reducing bacteria, we incubated marine sediments using an anoxic, continuous-flow bioreactor during two experiments at different advective porewater flow rates. We examined the growth kinetics of anaerobic methanotrophs and Desulfosarcina-like sulfate-reducing bacteria using quantitative PCR as a proxy for cell counts, and measured methane oxidation rates using membrane-inlet mass spectrometry. Our data show that the specific growth rates of ANME-1 and ANME-2 archaea differed in response to porewater flow rates. ANME-2 methanotrophs had the highest rates in lower-flow regimes (μANME-2 = 0.167 · week−1), whereas ANME-1 methanotrophs had the highest rates in higher-flow regimes (μANME-1 = 0.218 · week−1). In both incubations, Desulfosarcina-like sulfate-reducing bacterial growth rates were approximately 0.3 · week−1, and their growth dynamics suggested that sulfate-reducing bacterial growth might be facilitated by, but not dependent upon, an established anaerobic methanotrophic population. ANME-1 growth rates corroborate field observations that ANME-1 archaea flourish in higher-flow regimes. Our growth and methane oxidation rates jointly demonstrate that anaerobic methanotrophs are capable of attaining substantial growth over a range of environmental conditions used in these experiments, including relatively low methane partial pressures.

Transcriptomics analysis of the metabolic mechanisms of iron reduction induced by sulfate reduction mediated by sulfate-reducing bacteria

2021 ◽  
Author(s):  
Guo-Xiang Li ◽  
Peng Bao
Keyword(s):  
Gene Expression ◽  
Electron Transfer ◽  
Iron Reduction ◽  
Sulfate Reducing Bacteria ◽  
Sulfate Assimilation ◽  
Sulfate Reducing ◽  
Metabolic Characteristics ◽  
Pure Cultures ◽  
Reducing Bacteria

Abstract Sulfate-reducing bacteria (SRB) play an important role in sulfur, iron, and carbon cycling. The majority of studies have illustrated the role of SRB in biogeochemical cycling in pure cultures. In this study, we established three SRB enrichment cultures (designated HL, NB, and WC) from different paddy soils and conducted a transcriptomic analysis of their metabolic characteristics under sulfate and sulfate-free conditions. In the HL cultures, there was no sulfate consumption but ferrihydrite was reduced. This indicated that bacteria in the HL samples can reduce ferrihydrite and preferentially utilize ferrihydrite as the electron acceptor in the absence of both ferrihydrite and sulfate. Sulfate consumption was equal in the NB and the WC cultures, although more ferrihydrite was reduced in the NB cultures. Transcriptomics analysis showed that (i) upregulation of O-acetylserine sulfhydrylase gene expression indicating sulfate assimilation in the WC samples; (ii) the energy conservation trithionate pathway is commonly employed by SRB; (iii) sulfate not only enhanced iron reduction by its conversion to sulfide but also promoted enzymatic electron transfer via c-type cytochromes.

scholarly journals Effect of Quorum Sensing on the Ability of Desulfovibrio vulgaris To Form Biofilms and To Biocorrode Carbon Steel in Saline Conditions

2019 ◽  
Vol 86 (1) ◽  
Author(s):  
Giantommaso Scarascia ◽  
Robert Lehmann ◽  
Laura L. Machuca ◽  
Christina Morris ◽  
Ka Yu Cheng ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Carbon Steel ◽  
Quorum Sensing ◽  
Biofilm Formation ◽  
Sulfate Reducing Bacteria ◽  
Desulfovibrio Vulgaris ◽  
Content Type ◽  
Sulfate Reducing ◽  
Alternative Approach ◽  
Reducing Bacteria

ABSTRACT Sulfate-reducing bacteria (SRB) are key contributors to microbe-induced corrosion (MIC), which can lead to serious economic and environmental impact. The presence of a biofilm significantly increases the MIC rate. Inhibition of the quorum-sensing (QS) system is a promising alternative approach to prevent biofilm formation in various industrial settings, especially considering the significant ecological impact of conventional chemical-based mitigation strategies. In this study, the effect of the QS stimulation and inhibition on Desulfovibrio vulgaris is described in terms of anaerobic respiration, cell activity, biofilm formation, and biocorrosion of carbon steel. All these traits were repressed when bacteria were in contact with QS inhibitors but enhanced upon exposure to QS signal molecules compared to the control. The difference in the treatments was confirmed by transcriptomic analysis performed at different time points after treatment application. Genes related to lactate and pyruvate metabolism, sulfate reduction, electron transfer, and biofilm formation were downregulated upon QS inhibition. In contrast, QS stimulation led to an upregulation of the above-mentioned genes compared to the control. In summary, these results reveal the impact of QS on the activity of D. vulgaris, paving the way toward the prevention of corrosive SRB biofilm formation via QS inhibition. IMPORTANCE Sulfate-reducing bacteria (SRB) are considered key contributors to biocorrosion, particularly in saline environments. Biocorrosion imposes tremendous economic costs, and common approaches to mitigate this problem involve the use of toxic and hazardous chemicals (e.g., chlorine), which raise health and environmental safety concerns. Quorum-sensing inhibitors (QSIs) can be used as an alternative approach to inhibit biofilm formation and biocorrosion. However, this approach would only be effective if SRB rely on QS for the pathways associated with biocorrosion. These pathways would include biofilm formation, electron transfer, and metabolism. This study demonstrates the role of QS in Desulfovibrio vulgaris on the above-mentioned pathways through both phenotypic measurements and transcriptomic approach. The results of this study suggest that QSIs can be used to mitigate SRB-induced corrosion problems in ecologically sensitive areas.

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