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Abstract

Methane-oxidizing microorganisms perform an important role in reducing
emissions of the greenhouse gas methane to the atmosphere. To date,
known bacterial methanotrophs belong to the Proteobacteria,
Verrucomicrobia, and NC10 phyla. Within the Proteobacteria phylum, they
can be divided into type la, type Ib, and type II methanotrophs. Type la
and type II are well represented by isolates. Contrastingly, the vast
majority of type Ib methanotrophs have not been able to be cultivated so
far. Here, we compared the distributions of type Ib lineages in
different environments. Whereas the cultivated type Ib methanotrophs
(Methylococcus and Methylocaldum) are found in landfill and upland
soils, lineages that are not represented by isolates are mostly dominant
in freshwater environments, such as paddy fields and lake sediments.
Thus, we observed a clear niche differentiation within type Ib
methanotrophs. Our subsequent isolation attempts resulted in obtaining a
pure culture of a novel type Ib methanotroph, tentatively named
"Methylotetracoccus oryzae" C50C1. Strain C50C1 was further
characterized to be an obligate methanotroph, containing C-16(:1)omega
9c as the major membrane phospholipid fatty acid, which has not been
found in other methanotrophs. Genome analysis of strain C50C1 showed the
presence of two pmoCAB operon copies and XoxF5-type methanol
dehydrogenase in addition to MxaFI. The genome also contained genes
involved in nitrogen and sulfur cycling, but it remains to be
demonstrated if and how these help this type Ib methanotroph to adapt to
fluctuating environmental conditions in freshwater ecosystems.
IMPORTANCE Most of the methane produced on our planet gets naturally
oxidized by a group of methanotrophic microorganisms before it reaches
the atmosphere. These microorganisms are able to oxidize methane, both
aerobically and anaerobically, and use it as their sole energy source.
Although methanotrophs have been studied for more than a century, there
are still many unknown and uncultivated groups prevalent in various
ecosystems. This study focused on the diversity and adaptation of
aerobic methane-oxidizing bacteria in different environments by
comparing their phenotypic and genotypic properties. We used lab-scale
microcosms to create a countergradient of oxygen and methane for
preenrichment, followed by classical isolation techniques to obtain
methane-oxidizing bacteria from a freshwater environment. This resulted
in the discovery and isolation of a novel methanotroph with interesting
physiological and genomic properties that could possibly make this
bacterium able to cope with fluctuating environmental conditions.