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

Authors

  • Patricia L. Tavormina,

    Corresponding author
    1. Division of Geological and Planetary Sciences, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA 91125, USA.
      E-mail pattytav@gps.caltech.edu;
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  • Victoria J. Orphan,

    1. Division of Geological and Planetary Sciences, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA 91125, USA.
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  • Marina G. Kalyuzhnaya,

    1. Department of Microbiology, University of Washington, Box 355014, Seattle, WA 98115, USA.
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  • Mike S. M. Jetten,

    1. Department of Microbiology, Radboud University Nijmegen, 6525 AJ Nijmegen, The Netherlands.
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  • Martin G. Klotz

    Corresponding author
    1. Department of Biology, University of Louisville, 139 Life Sciences Building, Louisville, KY 40218, USA.
      E-mail martin.klotz@louisville.edu; Tel. (+1) 502 852 7779; Fax (+1) 502 852 0725.
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E-mail pattytav@gps.caltech.edu;

E-mail martin.klotz@louisville.edu; Tel. (+1) 502 852 7779; Fax (+1) 502 852 0725.

Summary

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.

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