A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs
Article first published online: 20 JUL 2010
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd
Environmental Microbiology Reports
Volume 3, Issue 1, pages 91–100, February 2011
How to Cite
Tavormina, P. L., Orphan, V. J., Kalyuzhnaya, M. G., Jetten, M. S. M. and Klotz, M. G. (2011), A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs. Environmental Microbiology Reports, 3: 91–100. doi: 10.1111/j.1758-2229.2010.00192.x
- Issue published online: 8 FEB 2011
- Article first published online: 20 JUL 2010
- Received 20 February, 2010; accepted 1 June, 2010.
Genomes of alphaproteobacterial and verrucomicrobial methane-oxidizing bacteria (MOB) encode sequence-divergent copies of particulate methane monooxygenase [pMMO = (PmoABC); pmoCAB]. In contrast, sequenced gammaproteobacterial MOB (Gamma-MOB) genomes contain single or multiple near-identical copies of pmoCAB operons. In betaproteobacterial ammonia-oxidizing bacteria (Beta-AOB), near-identical amoCAB operons encode ammonia monooxygenase (AMO), a homologue of pMMO. Here, we report that Gamma-MOB in the genera Methylomonas, Methylobacter and Methylomicrobium also encode a sequence-divergent particulate monooxygenase (pXMO). Whereas all known genes encoding pMMO or AMO cluster in the order ‘CAB’, the genes encoding pXMO are uniquely organized in the non-canonical form ‘pxmABC.’ Steady state pxm mRNA was detected in cultures of Methylomonas sp. as well as in freshwater creek sediment samples, demonstrating that pxm genes are expressed in culture and in situ. Inclusion of PxmA and PxmB proteins in phylogenetic analyses of the Pmo/Amo protein superfamilies created trifurcated trees with three major clades: (i) Pmo of Alpha- and Gamma-MOB and Amo of Gamma-AOB; (ii) Amo of Beta-AOB, Pmo of putative ethane-oxidizing Gamma-MOB and Pxm of Gamma-MOB; and (iii) verrucomicrobial Pmo and Amo of ammonia-oxidizing Archaea. These data support but do not prove the hypothesis that oxygen-dependent methane and ammonia monooxygenases evolved from a substrate-promiscuous ancestor after horizontal transfer while being integrated into the catabolic contexts of their extant hosts.