The membrane‐associated monooxygenase in the butane‐oxidizing Gram‐positive bacterium Nocardioides sp. strain CF8 is a novel member of the AMO/PMO family

Abstract

The Gram-positive bacterium Nocardioides sp. strain CF8 uses a membrane-associated monooxygenase (pBMO) to grow on butane. The nucleotide sequences of the genes encoding this novel monooxygenase were revealed through analysis of a de novo assembled draft genome sequence determined by high-throughput sequencing of the whole genome. The pBMO genes were in a similar arrangement to the genes for ammonia monooxygenase (AMO) from the ammonia-oxidizing bacteria and for particulate methane monooxygenase (pMMO) from the methane-oxidizing bacteria. The pBMO genes likely constitute an operon in the order bmoC, bmoA and bmoB. The nucleotide sequence was less than 50% similar to the genes for AMO and pMMO. The operon for pBMO was confirmed to be a single copy in the genome by Southern and computational analyses. In an incubation on butane the increase of transcriptional activity of the pBmoA gene was congruent with the increase of pBMO activity and suggested correspondence between gene expression and the utilization of butane. Phylogenetic comparison revealed distant but significant similarity of all three pBMO subunits to homologous members of the AMO/pMMO family and indicated that the pBMO represents a deeply branching third lineage of this group of particulate monooxygenases. No other bmoCAB-like genes were found to cluster with pBMO lineage in phylogenetic analysis by database searches including genomic and metagenomic sequence databases. pBMO is the first example of the AMO/pMMO-like monooxygenase from Gram-positive bacteria showing similarities to proteobacterial pMMO and AMO sequences.

Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers

“…Bacterial AMO display a high substrate flexibility and are well known for cometabolizing hydrocarbons (64), which is also reflected in the evolutionary relatedness of bacterial ammonia-and methane-monooxygenases (63,65). This finding is in line with the recent discovery of a novel monooxygenase from the AMO and pMMO family that catalyzes butane oxidation (66). As bacterial and archaeal ammonia monooxygenases are phylogenetically highly divergent, it is plausible that within the diversity of archaeal ammonia monooxygenases, some may in fact use substrates other than ammonia (67).…”

Gammaproteobacterial Methanotrophs Dominate Cold Methane Seeps in Floodplains of West Siberian Rivers

“…Remarkably, sequences related to the alkane monooxygenases of Nocardioides and Mycobacterium were amplified. They are only distantly related to known pmoA and amoA sequences, and the primer sets used in this study did not amplify alkane monooxygenase genes from pure cultures of Nocardioides and Mycobacterium (75,76). The fact that these sequences were obtained from the methane seep samples may be indicative of a high number of alkane oxidizers in these environments.…”

Hydrocarbon monooxygenase in Mycobacterium: recombinant expression of a member of the ammonia monooxygenase superfamily

“…Phylogenetic analyses, along with available physiological data, suggest that HmoCAB of NBB4 is a member of a functionally similar group of enzymes that are present in disparate heterotrophic Actinobacteria, where they enable opportunistic utilization of alkanes. Another member of this group is also likely to be present in the propane oxidizer Mycobacterium JOB5 (Hamamura et al, 1997(Hamamura et al, , 1999Sayavedra-Soto et al, 2011). Two aspects of genome relationships in this group are especially significant; the sequence divergence between these Actinobacterial CuMMOs is large relative to the ribosomal RNA divergence of the parent organisms, and available genome sequence data indicate the genes are not universally present among closely related bacteria.…”

“…In both strains, ATU inhibited butane growth and 14 C-labelled acetylene inhibited growth and resulted in labelling of a polypeptide corresponding to the size of a CuMMO subunit. Very recently, genes coding for a three-component monooxygenase with sequence homology to CuMMOs were reported in the draft genome sequence of Nocardioides CF8, and were transcribed in the presence of butane (Sayavedra-Soto et al, 2011). CuMMO sequences have also been linked to ethane-degrading organisms (Genbank accession number: BAH22836).…”