Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi

Boyd, Joel A.; Jungbluth, Sean P.; Leu, Andy O.; Evans, Paul N.; Woodcroft, Ben J; Chadwick, Grayson L.; Orphan, Victoria J.; Amend, Jan P.; Rappé, Michael S.; Tyson, Gene W.

doi:10.1101/390617

Cited by 17 publications

(19 citation statements)

References 70 publications

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“…In addition, the functional properties of the zm‐15 genome were examined with the KEGG database online (Kanehisa et al ., ). The heme motifs were predicted based on the conserved amino acid sequence of CxxCH (Boyd et al ., ) and the transmembrane domains were predicted using the TMHMM Server v. 2.0 (Moller et al ., ). The genome of the strain zm‐15 has been deposited in the NCBI databases under accession number of CP042908.…”

Section: Methodsmentioning

confidence: 99%

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Wang

Byrne

Liu

et al. 2020

Environ Microbiol Rep

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It has been recently shown that magnetite nanoparticles (nanoFe 3 O 4 ) can facilitate methanogenic syntrophy but the effect of magnetite on methanogenesis alone remains elusive. Here we show that aceticlastic methanogenesis by Methanosarcina mazei is accelerated by magnetite and is correlated with the redox cycling of structural Fe(II) and Fe(III) in the mineral. An enrichment and its closest pure culture relative, Ms. mazei zm-15, both obtained from a natural wetland of the Tibetan plateau were tested in this experiment. The Fe(II) to Fe(III) ratios in magnetite, as measured by multiple approaches, show an initial increase in both the methanogenic cultures and the blank preparations containing no microbes. The Fe(II)/Fe(III) ratio then displays a distinct decline followed by an increase towards the end of incubation only in the enrichment and pure culture cultivations. This redox cycling of magnetite is in accordance with the stimulation of aceticlastic methanogenesis. Microscopic observation reveals the precipitation of nanoFe 3 O 4 on methanogen cell surface. The genomic analysis predicts that in addition to electron transfer components essential for aceticlastic methanogenesis, Ms. mazei zm-15 contains an outer-surface multiheme c-type cytochrome (MHC) and a few function-unknown surface proteins that harbour monoheme motif. We hypothesize that the redox cycling of nanoFe 3 O 4 delivers a positive influence via the MHC to the membrane electron transfer chain and hence promote the aceticlastic methanogenesis.

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Section: Methodsmentioning

confidence: 99%

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Wang

Byrne

Liu

et al. 2020

Environ Microbiol Rep

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“…A beta-oxidation pathway showing similarity, based on the presence of genes similar to atoB, paaH, crt, and bcd/etf , to those described in the methanogenic Archaeoglobus was also observed in Ca. Lunaplasma lacustris (Boyd et al , 2019), so it is possible that these organisms degrade fatty acids for energy conservation (Figure 2; Supplemental Table 8). ORFs annotated as acetate-CoA ligase ( acd) were also present, possibly conferring the ability to produce ATP through fermentation (Schäfer et al , 1993) and providing another route for energy conservation in this apparently versatile population.…”

Section: Resultsmentioning

confidence: 99%

“…In RBG-13-57-23, nrfD was also located next to a formate dehydrogenase subunit ( fdhD ), and in RBG-19FT-COMBO-69-17, one nrfD was between a molybdopterin oxidoreductase encoding gene annotated as encoding tetrothionate reductase subunit A ( ttrA) and dmsB . Boyd et al (2019) found dmsB and nrfD located on the same operon in an Archaeoglobus MAG recovered from the deep subseafloor and posited that these genes encode proteins used in sulfur redox chemistry (Boyd et al , 2019). Similarly, sulfate-reducing organisms use NrfD-like proteins as electron shuttles during sulfate reduction (Pereira et al , 2011).…”

Section: Resultsmentioning

confidence: 99%

“…High-throughput sequencing of environmental DNA, metagenomic assembly of DNA sequence reads into contigs, and binning of contigs into metagenome-assembled genomes (MAGs) has provided unprecedented insights into the metabolic potential and evolutionary history of many uncultivated lineages (Hug et al , 2016; Brown et al , 2015; Woodcroft et al , 2018; Castelle et al , 2013; Crits-Christoph et al , 2018; Castelle et al , 2015; Anantharaman et al , 2016). In addition to revealing numerous new phyla, MAG analyses have identified new clades of microorganisms within longstanding phylogenetic groups, assigned biogeochemical roles to known but uncultivated lineages, and attributed new functions to diverse relatives of model prokaryotes (Graham et al , 2018; Mondav et al , 2014; Tully, 2019; Boyd et al , 2019; Solden et al , 2016; Singleton et al , 2018; Martinez et al , 2019). With these advances in sequencing technology, a more complex view of microbial evolution and metabolism has emerged.…”

Section: Introductionmentioning

confidence: 99%

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Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to theMethanomassiliicoccales

Zinke

Evans

Schroeder

et al. 2020

Preprint

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0Recent discoveries of mcr and mcr-like complexes in genomes from diverse archaeal 2 1 lineages suggest that methane (and more broadly alkane) metabolism is an ancient pathway with 2 2 complicated evolutionary histories. The conventional view is that methanogenesis is an ancestral 2 3 metabolism of the archaeal class Thermoplasmata. Through comparative genomic analysis of 12 2 4Thermoplasmata metagenome-assembled genomes (MAGs), we show that these microorganisms 2 5do not encode the genes required for methanogenesis, which suggests that this metabolism may 2 6 have been laterally acquired by an ancestor of the order Methanomassiliicoccales. These MAGs 2 7 include representatives from four orders basal to the Methanomassiliicoccales, including a high-2 8 quality MAG (95% complete) that likely represents a new order, Ca. Lunaplasma lacustris ord. 2 9 nov. sp. nov. These MAGs are predicted to use diverse energy conservation pathways, such as 3 0 heterotrophy, sulfur and hydrogen metabolism, denitrification, and fermentation. Two of these 3 1 lineages are globally widespread among anoxic, sedimentary environments, with the exception 3 2 of Ca. Lunaplasma lacustris, which has thus far only been detected in alpine caves and subarctic 3 3 lake sediments. These findings advance our understanding of the metabolic potential, ecology, 3 4 and global distribution of the Thermoplasmata and provide new insights into the evolutionary 3 5 history of methanogenesis within the Thermoplasmata. 3 6 3 7

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“…Bathyarchaeota and Ca. Syntrophoarchaeum 42 . Consistent with this, Co_bin109 encodes a Wood-Ljungdahl pathway (including carbon monoxide dehydrogenase / acetyl-CoA synthase complex) for complete fatty acid oxidation (Supplementary Table 6) .…”

Section: Resultsmentioning

confidence: 99%

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

Dong

Rattray

Campbell

et al. 2020

Preprint

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20At marine cold seeps, gaseous and liquid hydrocarbons migrate from deep subsurface 21 origins to the sediment-water interface. Cold seep sediments are known to host 22CoM reductase pathway), longer-chain alkanes (fumarate addition pathway), and 35 aromatic hydrocarbons (fumarate addition and subsequent benzoyl-CoA pathways), 36 including novel lineages within Methanosarcinales and Chloroflexi. Geochemical 37 profiling demonstrated that hydrocarbon substrates are abundant in this location, 38 thermogenic in origin, and subject to biodegradation. The detection of alkyl-39 /arylalkylsuccinate metabolites, together with carbon isotopic signatures of ethane, 40propane and carbon dioxide, support that microorganisms are actively degrading 41 hydrocarbons in these sediments. Capacities for reductive dehalogenation, sulfide 42 oxidation, hydrogen oxidation, carbon fixation, and fermentation are also widespread. 43Most community members may indirectly benefit from thermogenic hydrocarbons 44 through interspecies transfer of electrons and metabolites, and degradation of 45 necromass. Thus, we conclude that upward migrated thermogenic hydrocarbons are 46 important carbon and energy sources that sustain diverse subseafloor microbial 47 communities at permanently cold hydrocarbon seeps. 48 3 Introduction 49 Marine cold seeps are characterised by the migration of gas and oil from deep 50 subsurface sources to the sediment-water interface 1, 2 . This seepage often contains 51 gaseous short-chain alkanes, as well as heavier liquid alkanes and aromatic 52 compounds 3 , that originate from deep thermogenic petroleum deposits. Migrated 53 hydrocarbons can serve as an abundant source of carbon and energy for 54 microorganisms in these ecosystems, either via their direct utilization or indirectly 55 through metabolizing by-products of hydrocarbon biodegradation 4 . Multiple 16S rRNA 56 gene surveys have revealed that cold seep sediments at or near the sediment-water 57 interface host an extensive diversity of archaeal and bacterial lineages 5-9 . However, 58 much less is known about metabolic versatility of this diverse microbiome, and how 59 surface and subsurface populations are connected and differentiated in different redox 60 zones within the sediment column 10, 11 . Most seep-associated microorganisms lack 61 sequenced genomes, precluding meaningful predictions of relationships between 62 microbial lineages and their biogeochemical functions 4, 8, 10-13 . 63 Geochemical studies have provided evidence that microorganisms in deep seafloor 64 sediments, including cold seeps, mediate anaerobic hydrocarbon oxidation 2, 3 . A range 65 of efforts have been undertaken to enrich and isolate anaerobic hydrocarbon-oxidizing 66 microorganisms from cold seep sediments and other ecosystems rich in hydrocarbons 67 (e.g. marine hydrothermal vents) [5][6][7][8][9] 14 . Numerous studies have focused on anaerobic 68 oxidation of methane, since methane generally is the dominant hydrocarbon in cold 69 seep fluids. This process is mediated by...

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Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi

Cited by 17 publications

References 70 publications

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to theMethanomassiliicoccales

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

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