Stimulation of <i>Smithella</i>‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes

Xia, Xingxuan; Zhang, Jianchao; Song, Tianze; Lu, Yahai

doi:10.1111/1758-2229.12737

Cited by 56 publications

(29 citation statements)

References 84 publications

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“…We also showed that hydrogenotrophic methanogenesis is more abundant and active than methylotrophic methanogenesis. Since mangrove sediments are rich in organic carbon, hydrogenotrophic methanogens could consume H 2 and cooperate with syntrophic microbes to degrade short-chain fatty acids [44,45]. Co-occurrence analysis also revealed a significant non-random association of methanogens and Woesearchaeota.…”

Section: Discussionmentioning

confidence: 96%

Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments

et al. 2020

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Background: Methanogens are crucial to global methane budget and carbon cycling. Methanogens from the phylum Euryarchaeota are currently classified into one class and seven orders, including two novel methanogen taxa, Methanofastidiosa and Methanomassiliicoccales. The relative importance of the novel methanogens to methane production in the natural environment is poorly understood. Results: Here, we used a combined metagenomic and metatranscriptomic approach to investigate the metabolic activity of methanogens in mangrove sediments in Futian Nature Reserve, Shenzhen. We obtained 13 metagenome-assembled genomes (MAGs) representing one class (Methanofastidiosa) and five orders (Methanomassiliicoccales, Methanomicrobiales, Methanobacteriales, Methanocellales, and Methanosarcinales) of methanogens, including the two novel methanogens. Comprehensive annotation indicated the presence of an H 2dependent methylotrophic methanogenesis pathway in Methanofastidiosa and Methanomassiliicoccales. Based on the functional gene analysis, hydrogenotrophic and methylotrophic methanogenesis are the dominant pathways in mangrove sediments. MAG mapping revealed that hydrogenotrophic Methanomicrobiales were the most abundant methanogens and that methylotrophic Methanomassiliicoccales were the most active methanogens in the analyzed sediment profile, suggesting their important roles in methane production. Conclusions: Partial or near-complete genomes of two novel methanogen taxa, Methanofastidiosa and Methanomassiliicoccales, in natural environments were recovered and analyzed here for the first time. The presented findings highlight the ecological importance of the two novel methanogens and complement knowledge of how methane is produced in mangrove ecosystem. This study implies that two novel methanogens play a vital role in carbon cycle.

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Section: Discussionmentioning

confidence: 96%

Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments

et al. 2020

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“…In a coculture of Geobacter and Methanosarcina strains, the presence of magnetite significantly promoted syntrophic CH 4 production from ethanol and acetate oxidation (Tang et al ., ). A number of environmental enrichment studies have shown that addition of magnetite stimulates CH 4 production from syntrophic oxidation of ethanol, propionate, butyrate, phenol and complex aliphatic hydrocarbon (Kato et al ., ; Viggi et al ., ; Li et al ., ; Zhang and Lu ; Jing et al ., ; Fu et al ., ; Leitao et al ., ; Yan et al ., 2018; Xia et al ., ). It has been hypothesized that the effective electric conductivity of magnetite facilitates the direct interspecies electron transfer (DIET) for the syntrophy (Kato et al ., ; Viggi et al ., ; Li et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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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“…Syntrophomonas are not known to oxidize propionate but butyrate and up to C 10 fatty acids [43]. The inclusion of Syntrophomonas in analysis was due to the fact that Smithella, which utilize the C 6 dismutation pathway, can release butyrate as an intermediate product into environment, which is then metabolized by Syntrophomonas [44]. A total of 30 OTUs belonging to ve syntroph genera were retrieved.…”

Section: Resultsmentioning

confidence: 99%

“…Smithella in combination with Syntrophomonas are the next important group, while Syntrophobacter play only a minor role and that of Desulfotomaculum is negligible. Pelotomaculum and Smithella are known to use the methylmalonyl-CoA (MMC) pathway and the C 6 dismutation route, respectively [20,44,57,58]. Smithella are considered to tolerate a stricter thermodynamic condition than the MMC-utilizing syntrophs [59].…”

Section: Discussionmentioning

confidence: 99%

Thermodynamic Control on Biogeography and Functioning of Rare-Biosphere Propionate Syntrophs in Paddy Field Soils

Jin¹,

Jiao²,

Lu³

2020

Preprint

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Background Global biogeochemical processes are not only gauged by dominant taxa of soil microbiome but also depend on the critical functions of “rare biosphere” members. Here we evaluated the biogeographical pattern of “rare biosphere” propionate-oxidizing syntrophs in 113 paddy soil samples collected across eastern China. Results The relative abundance, functioning capacity and growth potential of propionate-oxidizing syntrophs were analyzed to provide a panoramic view of syntroph biogeographical distribution at the continental scale. The relative abundances of four syntroph genera, Syntrophobacter, Pelotomaculum, Smithella and Syntrophomonas were significantly greater at the warm low latitudes than at the cool high latitudes. Correspondingly, the functioning potential of propionate degradation was greater in the low latitude soils compared with the high latitude soils. The slow rate of propionate degradation in high latitude soils resulted in a greater fold change in increase of the relative abundance, probably due to the growth rate-yield tradeoff relationship. The mean annual temperature (MAT) is the most important factor shaping the biogeographical pattern of propionate-oxidizing syntrophs, with the next factor to be the total S content (TS) in soil. Conclusions We suggest that the effect of MAT is related to the Gibbs free energy change, in which the endergonic tension of propionate oxidation is leveraged with the increase of MAT. The TS effect is likely due to that some propionate syntrophs can facultatively perform sulfate respiration.

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Stimulation of Smithella‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes

Cited by 56 publications

References 84 publications

Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments

Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments

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

Thermodynamic Control on Biogeography and Functioning of Rare-Biosphere Propionate Syntrophs in Paddy Field Soils

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