Diverse bacteriohemerythrin genes ofMethylomonas denitrificansFJG1 provide insight into the survival and activity of proteobacterial methanotrophs under hypoxia

Abstract

AbstractProteobacterial methanotrophic bacteria are dependent on the oxidation of methane and methanol for the assimilation of carbon. Interestingly, these types of methanotrophs can thrive in oxygen-depleted zones of lakes and other aquatic ecosystems despite the fact they are considered obligate aerobes. Bacteriohemerythrin (Bhr), a homologue of eukaryotic hemerythrin, is a protein associated with oxygen binding. The model gammaproteobacterial methanotrophic strain,Methylomonas denitrificansFJG1, oxidizes methane at the expense of nitrate reduction under extreme hypoxia and upregulatesbhrgenes, yet this strain encodes 10 homologues ofbhrin its genome. UsingM. denitrificansFJG1 as a model, this study examined the prevalence and phylogeny of each of its 10bhrhomologues in other methanotroph and general bacterial genomes. One gene copy denoted as “bhr-00” was found to be methanotroph-specific, was upregulated under hypoxia inM. denitrificansFJG1, and was predicted to have a structure nearly identical to the crystalized, oxygen-scavenging, Bhr-Bath protein from,Methylococcus capsulatusBath. Other upregulatedbhrgenes from hypoxic cultures of nitrate-grownM. denitrificansFJG1 included those with gene neighborhoods related to oxygen sensing, denitrification and chemotaxis. Together, this study uncovered multifunctional roles of bacteriohemerythrin proteins encoded and expressed by methanotrophs that likely enable their survival in hypoxic ecosystems.ImportanceAerobic gammaproteobacterial methanotrophs encoding bacteriohemerythrin (bhr) genes are reported to have an enhanced ability to survive and grow in oxygen-limited environments. The methanotrophic bacterium,Methylomonas denitrificansFJG1, encodes 10 copies ofbhrgenes, of which 7 are expressed under oxygen depleted and denitrifying conditions. Comparing these 10bhrgene homologues fromM. denitrificansFJG1 with those from other prokaryotic genomes revealed that copy “bhr-00” is nearly exclusive to methanotrophs. Gene neighbourhoods surrounding conservedbhrgene sequences in methanotroph genomes suggest a range of potential functions including oxygen sensing and delivery, chemotaxis, and nitrate reduction. The results from this study illuminate a previously undescribed diversity of the structure and function ofbhrgenes inM. denitrificansFJG1 and related methanotrophic bacteria and pinpoints roles of Bhr that likely promote survival of methanotrophs in hypoxic ecosystems.