Novel copper-containing membrane monooxygenases (CuMMOs) encoded by alkane-utilizing Betaproteobacteria

Rochman, Fauziah F.; Kwon, Miye; Khadka, Roshan; Tamas, Ivica; Lopez-Jauregui, Azriel Abraham; Sheremet, Andriy; V. Smirnova, Angela; Malmstrom, Rex R.; Yoon, Sukhwan; Woyke, Tanja; Dunfield, Peter F.; Verbeke, Tobin J.

doi:10.1038/s41396-019-0561-2

Title: Novel copper-containing membrane monooxygenases (CuMMOs) encoded by alkane-utilizing Betaproteobacteria

Journal Article · 02 December 2019 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-019-0561-2 · OSTI ID:1597723

Rochman, Fauziah F. ^[1]; Kwon, Miye ^[2]; Khadka, Roshan ^[1]; Tamas, Ivica ^[3];

^[4]; Sheremet, Andriy ^[1]; V. Smirnova, Angela ^[1]; Malmstrom, Rex R. ^[5]; Yoon, Sukhwan ^[2];

^[5];

^[1];

^[1]

Univ. of Calgary, AB (Canada)
Korea Inst. of Science and Technology, Daejeon (Korea)
Univ. of Calgary, AB (Canada); Univ. of Novi Sad (Serbia)
Univ. of Calgary, AB (Canada); Inst. Tecnologico y de Estudios Superiores de Monterrey, Chihuahua (Mexico)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Copper-containing membrane monooxygenases (CuMMOs) are encoded by xmoCAB(D) gene clusters and catalyze the oxidation of methane, ammonia, or some short-chain alkanes and alkenes. In a metagenome constructed from an oilsands tailings pond we detected an xmoCABD gene cluster with <59% derived protein sequence identity to genes from known bacteria. Stable isotope probing experiments combined with a specific xmoA qPCR assay demonstrated that the bacteria possessing these genes were incapable of methane assimilation, but did grow on ethane and propane. Single-cell amplified genomes (SAGs) from propane-enriched samples were screened with the specific PCR assay to identify bacteria possessing the target gene cluster. Multiple SAGs of Betaproteobacteria belonging to the genera Rhodoferax and Polaromonas possessed homologues of the metagenomic xmoCABD gene cluster. Unexpectedly, each of these two genera also possessed other xmoCABD paralogs, representing two additional lineages in phylogenetic analyses. Metabolic reconstructions from SAGs predicted that neither bacterium encoded enzymes with the potential to support catabolic methane or ammonia oxidation, but that both were capable of higher n-alkane degradation. The involvement of the encoded CuMMOs in alkane oxidation was further suggested by reverse transcription PCR analyses, which detected elevated transcription of the xmoA genes upon enrichment of water samples with propane as the sole energy source. Enrichments, isotope incorporation studies, genome reconstructions, and gene expression studies therefore all agreed that the unknown xmoCABD operons did not encode methane or ammonia monooxygenases, but rather n-alkane monooxygenases. Finally, this study broadens the known diversity of CuMMOs and identifies these enzymes in non-nitrifying Betaproteobacteria.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Natural Sciences and Engineering Research Council of Canada (NSERC); National Research Foundation of Korea

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1597723

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 3 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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