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A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs

Tavormina, Patricia L. and Orphan, Victoria J. and Kalyuzhnaya, Marina G. and Jetten, Mike S. M. and Klotz, Martin G. (2011) A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs. Environmental Microbiology Reports, 3 (1). pp. 91-100. ISSN 1758-2229. https://resolver.caltech.edu/CaltechAUTHORS:20110308-093513808

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/j.1758-2229.2010.00192.x DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/j.1758-2229.2010.00192.x/abstractPublisherArticle
ORCID:
AuthorORCID
Orphan, Victoria J.0000-0002-5374-6178
Kalyuzhnaya, Marina G.0000-0002-9058-7794
Jetten, Mike S. M.0000-0002-4691-7039
Additional Information:© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd. Received 20 February, 2010; accepted 1 June, 2010. Article first published online: 20 Jul. 2010. We thank Dan Arp for providing genomic DNA from Nitrosomonas europaea, and Burt Thomas for peat bog samples. We also thank three anonymous reviewers for critical reading of this manuscript. Funding for this project was provided by the Gordon and Betty Moore Foundation, and from National Aeronautics Space Administration grant NNF06GB34G (VJO), UW Royalty Research Fund grant 4064 and NSF Grant MCB-0604269 (M.G. Kalyuzhnaya), ERC Advanced Grant 232937 (MSMJ) and the Office of the EVP Research of UofL (M.G. Klotz).
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationUNSPECIFIED
NASANNF06GB34G
UW Royalty Research Fund4064
NSFMCB-0604269
European Research Council (ERC)232937
Office of the EVP Research of UofLUNSPECIFIED
Issue or Number:1
Record Number:CaltechAUTHORS:20110308-093513808
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110308-093513808
Official Citation: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
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:22708
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:08 Mar 2011 18:07
Last Modified:09 Mar 2020 13:18

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