Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea

Yu, Hang; Susanti, Dwi; McGlynn, Shawn E.; Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder; Scheller, Silvan; Tavormina, Patricia L.; Hettich, Robert L.; Mukhopadhyay, Biswarup; Orphan, Victoria J.

doi:10.3389/fmicb.2018.02917

Cited by 42 publications

(79 citation statements)

References 98 publications

(164 reference statements)

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“…ANME-1 have been proposed to couple AOM to the reduction of polysulfide in a biogenic hydrocarbon seep sediment, but this was based on the annotation and high expression of a putative sulfide: quinone oxidoreductase (SQR)(67). Genes for dissimilatory sulfate reduction pathways were absent in the Methanoperedenaceae MAGs, consistent with other ANME lineages (68). MGW-1 was recently speculated to directly couple AOM to sulfate reduction utilising assimilatory sulfate reduction pathways.…”

Section: Resultssupporting

confidence: 81%

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Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

McIlroy

Leu

et al. 2020

Preprint

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Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceace metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate, and the reduction of arsenate, selenate and elemental sulfur. Numerous membrane-bound multi-heme c type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humics and syntrophic partners.ImportanceAOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance to the global carbon cycle and climate change modelling. While the oxidation of methane coupled to sulphate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae as they are absent in related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.

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Section: Resultssupporting

confidence: 81%

“…This hypothesis was based on the lack of large MHCs or identifiable alternate electron acceptor complexes encoded in the MAG (29). Several of the Methanoperedenaceae MAGs, and those of other ANME lineages, contain candidate genes associated with assimilatory sulfate reduction, but a dissimilatory role for these has not been shown (68).…”

Section: Resultsmentioning

confidence: 99%

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

McIlroy

Leu

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…ANME-1 has been proposed to couple AOM to the reduction of polysulfide in a biogenic hydrocarbon seep sediment, but this was based on the annotation and high expression of a putative sulfide: quinone oxidoreductase (SQR) (65). Genes for dissimilatory sulfate reduction pathways were absent in the Methanoperedenaceae MAGs, consistent with other ANME lineages (66). MGW-1 was recently speculated to directly couple AOM to sulfate reduction by utilizing assimilatory sulfate reduction pathways.…”

Section: Resultsmentioning

confidence: 99%

“…This hypothesis was based on the lack of large MHCs or identifiable alternate electron acceptor complexes encoded in the MAG (30). Several of the Methanoperedenaceae MAGs, and those of other ANME lineages, contain candidate genes associated with assimilatory sulfate reduction, but a dissimilatory role for these has not been shown (66).…”

Section: Resultsmentioning

confidence: 99%

Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae

Leu

McIlroy

et al. 2020

mBio

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Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.

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“…The up-regulation of genes in sulfur metabolism could improve the generation of 3'-phosphoadenosine 5'-phosphosulfate (PAPS) and sul de. PAPS is a sulfate donor for many sulfating reactions and sul de is an important material for the biosynthesis of cysteine [38]. This indicated that the synthesis of PHB could promote the creation of sulfur-containing compounds and cysteine.…”

Section: Transcriptomic Evidences Of the Stimulating Effect Of Polyhymentioning

confidence: 99%

Increasing Ascomycin Yield in Streptomyces Hygroscopicus var. Ascomyceticus by Using Polyhydroxybutyrate as an Intracellular Carbon Supply Station

Wang

Yin

Wang

et al. 2020

Preprint

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Background: Ascomycin is a multifunctional antibiotic produced by Streptomyces hygroscopicus var. ascomyceticus. As a secondary metabolite, the production of ascomycin is often limited by the shortage of precursors during the late fermentation phase. Polyhydroxybutyrate is an intracellular polymer accumulated by various microorganisms. The development of polyhydroxybutyrate as a useful carbon reservoir for precursor synthesis is of great significance for improving the yield of ascomycin.Results: The fermentation characteristics of the parent strain S. hygroscopicus var. ascomyceticus FS35 showed that the accumulation and decomposition of polyhydroxybutyrate were respectively correlated with the growth of strain and the production of ascomycin. The co-overexpression of exogenous polyhydroxybutyrate synthesis gene phaC and native polyhydroxybutyrate decomposition gene fkbU increased both strain biomass and ascomycin yield. Comparative transcription analysis showed that the storage of polyhydroxybutyrate during the exponential phase accelerated biosynthesis processes by stimulating the utilization of carbon sources, and the decomposition of polyhydroxybutyrate during the stationary phase increased the biosynthesis of ascomycin precursors by enhancing metabolic flux of primary pathways. The comparative analysis of cofactor concentration reflected that the biosynthesis of polyhydroxybutyrate depended on the supply of NADH pool. Under the condition of low sugar content in the later exponential phase, the optimization of carbon source addition further strengthened the polyhydroxybutyrate metabolism by increasing total concentration of cofactors. Finally, in the fermentation medium with 22 g/L starch and 52 g/L dextrin, the ascomycin yield of co-overexpression strain was increased to 626.30 mg/L, 2.11-fold higher than that of parent strain in the initial medium (296.29 mg/L). Conclusions: This paper reported for the first time that the polyhydroxybutyrate was beneficial to the growth of strain and the production of ascomycin by working as an intracellular carbon reservoir, storing as polymers when carbon sources are abundant and depolymerizing to monomers for the biosynthesis of precursors when carbon sources are insufficient. The successful application of polyhydroxybutyrate in increasing the output of ascomycin provided a new strategy for the high yield of other secondary metabolites.

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Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea

Cited by 42 publications

References 98 publications

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae

Increasing Ascomycin Yield in Streptomyces Hygroscopicus var. Ascomyceticus by Using Polyhydroxybutyrate as an Intracellular Carbon Supply Station

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