Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov.

Bodrossy, Levente; Holmes, E. M.; Holmes, Andrew; Kovács, Kornél L.; Murrell, J. Colin

doi:10.1007/s002030050527

Cited by 190 publications

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“…One additional type of gammaproteobacterial methanotrophs, type X, was originally proposed for Methylococcus capsulatus, which, in addition to ribulose monophosphate pathway, possesses ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO), a key enzyme in the Calvin-Benson cycle (Whittenbury and Dalton, 1981;Whittenbury, 1981). Several Methylococcus-related methanotrophs have been described including the genera Methylocaldum (Bodrossy et al, 1997;Takeuchi et al, 2014), Methyloparacoccus (Hoefman et al, 2014) and Methylogaea (Geymonat et al, 2010). Members of these genera form a monophyletic cluster in pmoA gene-based trees and are lately addressed as type Ib methanotrophs.…”

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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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“…In the last 10 years, novel cultivation techniques have enabled the isolation of previously uncultured methane oxidizers; the characterization of these new genera has led to an improved understanding of methanotroph taxonomy (Bowman et al, 1993(Bowman et al, , 1997Bodrossy et al, 1997;Dedysh et al, 1998Dedysh et al, , 2000Dedysh et al, , 2002Wise et al, 1999Wise et al, , 2001. Methanotrophs are currently classified as type I methanotrophs (comprising nine genera among the g-proteobacteria) and type II methanotrophs (comprising four genera among the a-proteobacteria), according to their intracytoplasmic membrane structure, carbon assimilation pathways, fatty acid composition and phylogeny (Hanson and Hanson, 1996).…”

Section: Introductionmentioning

confidence: 99%

Effect of earthworms on the community structure of active methanotrophic bacteria in a landfill cover soil

et al. 2007

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In the United Kingdom, landfills are the primary anthropogenic source of methane emissions. Methanotrophic bacteria present in landfill biocovers can significantly reduce methane emissions via their capacity to oxidize up to 100% of the methane produced. Several biotic and abiotic parameters regulate methane oxidation in soil, such as oxygen, moisture, methane concentration and temperature. Earthworm-mediated bioturbation has been linked to an increase in methanotrophy in a landfill biocover soil (AC Singer et al., unpublished), but the mechanism of this trophic interaction remains unclear. The aims of this study were to determine the composition of the active methanotroph community and to investigate the interactions between earthworms and bacteria in this landfill biocover soil where the methane oxidation activity was significantly increased by the earthworms. Soil microcosms were incubated with 13 C-CH 4 and with or without earthworms. DNA and RNA were extracted to characterize the soil bacterial communities, with a particular emphasis on methanotroph populations, using phylogenetic (16S ribosomal RNA) and functional methane monooxygenase (pmoA and mmoX) gene probes, coupled with denaturing gradient-gel electrophoresis, clone libraries and pmoA microarray analyses. Stable isotope probing (SIP) using 13 C-CH 4 substrate allowed us to link microbial function with identity of bacteria via selective recovery of 'heavy' 13 C-labelled DNA or RNA and to assess the effect of earthworms on the active methanotroph populations. Both types I and II methanotrophs actively oxidized methane in the landfill soil studied. Results suggested that the earthworm-mediated increase in methane oxidation rate in the landfill soil was more likely to be due to the stimulation of bacterial growth or activity than to substantial shifts in the methanotroph community structure. A Bacteroidetes-related bacterium was identified only in the active bacterial community of earthworm-incubated soil but its capacity to actually oxidize methane has to be proven.

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“…The type I methanotrophs have been taxonomically united to form the family Methylococcaceae, of which four genera were originally distinguished on the basis of phospholipid fatty acid patterns, 16S rDNA analysis and phenotypic traits : Methylococcus, Methylomonas, Methylobacter, Methylomicrobium (Bowman et al, 1993, 1995. More recently, the ecological and phylogenetic diversity of the Methylococcaceae has expanded considerably as members of a psychrophilic genus, Methylosphaera (Bowman et al, 1997), and thermophilic genera, Methylocaldum and ' Methylothermus ' (Bodrossy et al, 1997(Bodrossy et al, , 1999, have been described.Previously, we reported on the use of an extinctiondilution enrichment method to isolate novel methanotrophs from landfill cover soil in the southeastern USA (Wise et al, 1999). 16S rDNA analysis of two type I isolates, designated AML-C10 T and AML-D4 T , showed that they were members of a novel methanotrophic phylotype as defined by clone sequences retrieved from directly extracted soil DNA.…”

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Methylosarcina fibrata gen. nov., sp. nov. and Methylosarcina quisquiliarum sp.nov., novel type 1 methanotrophs.

Wise¹,

McArthur²,

Shimkets³

2001

International Journal of Systematic and Evolutionary Microbiology

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Two novel species of obligate methane-oxidizing bacteria, isolated from landfill soil, were characterized. Both strains were unusual in that some members of the population grew in irregularly shaped, refractile cell packets that resembled sarcina-like clusters. Electron microscopy revealed that the cell packets were covered with a slime layer and the cells contained many large granular inclusion bodies. The individual cells of each strain were sometimes motile and had differing morphologies. Isolate AML-C10 T was always coccoidal in shape, and the cells were covered with extracellular fibrils. Isolate AML-D4 T was pleomorphic, changing from rod to coccal form, sometimes exhibiting an unusual fusiform morphology. AML-D4T lacked the extensive fibrillar matrix observed with AML-C10 T . Both strains utilized only methane and methanol as carbon sources. In stationary phase, the cells of each strain swelled in size and formed cysts. Aside from morphological differences, strains could also be distinguished from each other by cellular protein patterns, as well as by temperature and pH tolerances. 16S rDNA phylogenetic analysis showed that these are type I methanotrophs (family : Methylococcaceae) most closely related to the Methylobacter/Methylomicrobium clade, although they form a monophyletic grouping supported by moderately high bootstrap values. By 16S rDNA database searches, the most similar species to both isolates were Methylobacter spp. However, partial particulate methane monooxygenase sequence analysis suggested that these bacteria might be more closely related to Methylomicrobium than Methylobacter. Furthermore, cellular fatty acid profiles of the strains more closely resemble those of Methylomicrobium, although the absence of significant levels of 16 :1ω5c argues for the uniqueness of these two strains. On the basis of the results described here, it is proposed that a new genus should be created, Methylosarcina gen. nov., harbouring two species, Methylosarcina fibrata sp. nov. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and partial pmoA sequence of AML-C10T and AML-D4 T are AF177296 and AF177325, and AF177297 and AF177326, respectively. methanotrophs, play a key role in the global consumption of methane (Hanson, 1998 ;King, 1992). Methane is efficient at absorbing and re-emitting infrared radiation, and its accumulation contributes to global warming (Topp & Hanson, 1991). Methanotrophs are also of interest due to their ability to degrade some environmental contaminants, like the common solvent trichloroethylene (DiSpirito et al., 1992 ;Tsien et al., 1989). Methane-oxidizing bacteria have historically been divided into two groups, the type I and the type II methanotrophs, based primarily on their biochemistry, morphological features and phylogenetic placement (Hanson & Hanson, 1996). 16S rRNA sequence analysis of the type I (or group I) methanotrophs shows them to form a coherent cluster within the γ-subclass of the Proteobacteria (Bowman et al., 1995). These bacteria utilize the ribulose monopho...

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Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov.

Cited by 190 publications

References 0 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

Effect of earthworms on the community structure of active methanotrophic bacteria in a landfill cover soil

Methylosarcina fibrata gen. nov., sp. nov. and Methylosarcina quisquiliarum sp.nov., novel type 1 methanotrophs.

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