Distribution and diversity of <scp><i>V</i></scp><i>errucomicrobia</i> methanotrophs in geothermal and acidic environments

Sharp, Christine E.; Smirnova, Angela V.; Graham, Jaime M.; Stott, Matthew B.; Khadka, Roshan; Moore, Tim R.; Grasby, Stephen E.; Strack, Maria; Dunfield, Peter F.

doi:10.1111/1462-2920.12454

Cited by 130 publications

(129 citation statements)

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“…The latter were only recently discovered and appear to be restricted to acidic geothermal environments (Sharp et al, 2014). By contrast, methanotrophic proteobacteria occur in a wide range of habitats where both methane and oxygen are available (Nazaries et al, 2013) and affiliate with the classes Gammaproteobacteria (type I methanotrophs) and Alphaproteobacteria (type II methanotrophs).…”

Section: Introductionmentioning

confidence: 99%

A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments

et al. 2016

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Although representatives with spiral-shaped cells are described for many functional groups of bacteria, this cell morphotype has never been observed among methanotrophs. Here, we show that spiral-shaped methanotrophic bacteria do exist in nature but elude isolation by conventional approaches due to the preference for growth under micro-oxic conditions. The helical cell shape may enable rapid motility of these bacteria in water-saturated, heterogeneous environments with high microbial biofilm content, therefore offering an advantage of fast cell positioning under desired high methane/low oxygen conditions. The pmoA genes encoding a subunit of particulate methane monooxygenase from these methanotrophs form a new genus-level lineage within the family Methylococcaceae, type Ib methanotrophs. Application of a pmoA-based microarray detected these bacteria in a variety of high-latitude freshwater environments including wetlands and lake sediments. As revealed by the environmental pmoA distribution analysis, type Ib methanotrophs tend to live very near the methane source, where oxygen is scarce. The former perception of type Ib methanotrophs as being typical for thermal habitats appears to be incorrect because only a minor proportion of pmoA sequences from these bacteria originated from environments with elevated temperatures.

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Section: Introductionmentioning

confidence: 99%

A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments

et al. 2016

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“…The three thermophilic strains belonging to the genus Methylacidiphilum share low pH optima (2 to 3.5) and high temperature optima (55 to 60°C) (7). In addition, 16S rRNA gene sequences from different geothermal sites showed identities of only 95% to 99% to the 16S rRNA gene sequence of M. fumariolicum SolV (8,14,16). This indicated that a larger diversity in verrucomicrobial methanotrophs might exist in geothermal environments.…”

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confidence: 97%

“…Like most other aerobic methane oxidizers, the Verrucomicrobia use particulate methane monooxygenase (pMMO) to catalyze the first step of the methane oxidation. Unlike most proteobacterial methanotrophs (7), but like Methylomirabilis oxyfera (belonging to the NC10 phylum) (12), M. fumariolicum SolV (13) and M. infernorum V4 (14) grow as autotrophs, using only carbon dioxide as the carbon source via the Calvin cycle.All verrucomicrobial methanotrophs known to date have been enriched from geothermal environments (7,15,16), and 16S rRNA gene surveys indicated their presence to be mainly limited to such environments (16). The three thermophilic strains belonging to the genus Methylacidiphilum share low pH optima (2 to 3.5) and high temperature optima (55 to 60°C) (7).…”

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confidence: 99%

Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov

Teeseling

Pol

Harhangi

et al. 2014

Appl Environ Microbiol

172

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Methanotrophic Verrucomicrobia have been found in geothermal environments characterized by high temperatures and low pH values. However, it has recently been hypothesized that methanotrophic Verrucomicrobia could be present under a broader range of environmental conditions. Here we describe the isolation and characterization of three new species of mesophilic acidophilic verrucomicrobial methanotrophs from a volcanic soil in Italy. The three new species showed 97% to 98% 16S rRNA gene identity to each other but were related only distantly (89% to 90% on the 16S rRNA level) to the thermophilic genus Methylacidiphilum. We propose the new genus Methylacidimicrobium, including the novel species Methylacidimicrobium fagopyrum, Methylacidimicrobium tartarophylax, and Methylacidimicrobium cyclopophantes. These mesophilic Methylacidimicrobium spp. were more acid tolerant than their thermophilic relatives; the most tolerant species, M. tartarophylax, still grew at pH 0.5. The variation in growth temperature optima (35 to 44°C) and maximum growth rates (max; 0.013 to 0.040 h ؊1 ) suggested that all species were adapted to a specific niche within the geothermal environment. All three species grew autotrophically using the Calvin cycle. The cells of all species contained glycogen particles and electron-dense particles in their cytoplasm as visualized by electron microscopy. In addition, the cells of one of the species (M. fagopyrum) contained intracytoplasmic membrane stacks. The discovery of these three new species and their growth characteristics expands the known diversity of verrucomicrobial methanotrophs and shows that they are present in many more ecosystems than previously assumed. Methane oxidation is a microbial process which limits the amount of methane released to the atmosphere (1). Microbial methane oxidation can occur via different routes, including either anaerobically (2, 3, 4) or aerobically (5, 6, 7). The diversity of the biochemistry of methane oxidation is also reflected in the diversity of organisms performing these processes. For a long time, Alpha-and Gammaproteobacteria were considered to be the only organisms to perform aerobic methane oxidation. However, in 2007, methane-oxidizing Verrucomicrobia were discovered (genus Methylacidiphilum [8, 9, 10]); also, intra-aerobic bacteria belonging to the NC10 candidate phylum (3, 11) were recently described to oxidize methane using internally produced oxygen. Like most other aerobic methane oxidizers, the Verrucomicrobia use particulate methane monooxygenase (pMMO) to catalyze the first step of the methane oxidation. Unlike most proteobacterial methanotrophs (7), but like Methylomirabilis oxyfera (belonging to the NC10 phylum) (12), M. fumariolicum SolV (13) and M. infernorum V4 (14) grow as autotrophs, using only carbon dioxide as the carbon source via the Calvin cycle.All verrucomicrobial methanotrophs known to date have been enriched from geothermal environments (7,15,16), and 16S rRNA gene surveys indicated their presence to be mainly limited to such env...

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“…However, more recently, a number of type II methanotrophs (Methylocella, Methylocapsa, and Methylocystis) have been characterized as facultative methanotrophs capable of conserving energy for growth on multicarbon compounds such as acetate, pyruvate, succinate, malate, and ethanol (12). Although members of the phylum Verrucomicrobia have been widely detected in peatlands, none has been definitively linked to methanotrophy, and thus more research is needed to ascertain the role of Verrucomicrobia in the carbon cycle of peatlands (8,13,14,15,16).Aerobic methane oxidation in proteobacterial methanotrophs is catalyzed by the enzyme methane monooxygenase (MMO), either particulate MMO (pMMO) or a soluble MMO (sMMO). The genes pmoA (encoding the 27-kDa subunit of pMMO) and mmoX (encoding the alpha-subunit of the hydroxylase of sMMO) as well as 16S rRNA genes have been used most often as molecular markers to characterize methanotrophs in peatlands and other environments (6,17,18,19,20,21,22,23).…”

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confidence: 99%

mentioning

confidence: 99%

Alpha- and Gammaproteobacterial Methanotrophs Codominate the Active Methane-Oxidizing Communities in an Acidic Boreal Peat Bog

Esson

Kumaresan

et al. 2016

Appl Environ Microbiol

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dThe objective of this study was to characterize metabolically active, aerobic methanotrophs in an ombrotrophic peatland in the Marcell Experimental Forest, in Minnesota. Methanotrophs were investigated in the field and in laboratory incubations using DNA-stable isotope probing (SIP), expression studies on particulate methane monooxygenase (pmoA) genes, and amplicon sequencing of 16S rRNA genes. Potential rates of oxidation ranged from 14 to 17 mol of CH 4 g dry weight soil ؊1 day ؊1 . Within DNA-SIP incubations, the relative abundance of methanotrophs increased from 4% in situ to 25 to 36% after 8 to 14 days. Phylogenetic analysis of the 13 C-enriched DNA fractions revealed that the active methanotrophs were dominated by the genera Methylocystis (type II; Alphaproteobacteria), Methylomonas, and Methylovulum (both, type I; Gammaproteobacteria). In field samples, a transcript-to-gene ratio of 1 to 2 was observed for pmoA in surface peat layers, which attenuated rapidly with depth, indicating that the highest methane consumption was associated with a depth of 0 to 10 cm. Metagenomes and sequencing of cDNA pmoA amplicons from field samples confirmed that the dominant active methanotrophs were Methylocystis and Methylomonas. Although type II methanotrophs have long been shown to mediate methane consumption in peatlands, our results indicate that members of the genera Methylomonas and Methylovulum (type I) can significantly contribute to aerobic methane oxidation in these ecosystems. Methane is the third most important greenhouse gas and has 28 times the potential of carbon dioxide to trap heat radiation on a molecular basis over a 100-year time scale (1, 2, 3). Wetlands, such as peatlands, represent the largest natural source of methane to the atmosphere (4). Aerobic methanotrophic bacteria live at the oxic-anoxic interface of wetland soils, and it has been shown that they consume as much as 90% of the methane produced belowground before it reaches the atmosphere, thus serving as a biofilter regulating emissions (3, 5, 6, 7). The response of methane dynamics in wetlands to global climate change is uncertain, and climate models would be improved through quantification of the response of microbially mediated mechanisms of methanotrophy to temperature and moisture variation.Aerobic methanotrophs are phylogenetically located in two phyla: the Proteobacteria and Verrucomicrobia (8). The majority of characterized methane-oxidizing organisms have been separated into type I methanotrophs of the Gammaproteobacteria and type II methanotrophs of the Alphaproteobacteria (9, 10, 11). The prevailing view has been that most methanotrophs grow only on methane or methanol as a source of carbon and energy (4). However, more recently, a number of type II methanotrophs (Methylocella, Methylocapsa, and Methylocystis) have been characterized as facultative methanotrophs capable of conserving energy for growth on multicarbon compounds such as acetate, pyruvate, succinate, malate, and ethanol (12). Although members of the phylum Verrucomic...

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Distribution and diversity of Verrucomicrobia methanotrophs in geothermal and acidic environments

Cited by 130 publications

References 48 publications

A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments

A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments

Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov

Alpha- and Gammaproteobacterial Methanotrophs Codominate the Active Methane-Oxidizing Communities in an Acidic Boreal Peat Bog

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