Samuel Imisi Awala1, Joo-Han Gwak1, Yong-Man Kim1, So-Jeong Kim2, Andrea Strazzulli3, Peter F. Dunfield4, Hyeokjun Yoon5, Geun-Joong Kim6 and Sung-Keun Rhee1,*
1Department of Biological Sciences and Biotechnology, Chungbuk National University, 1 Chungdae-ro, Seowon-Gu, Cheongju 28644, Republic of Korea. 2Geologic Environment Research Division, Korea Institute of Geoscience and Mineral Resources, Daejeon 34132, Republic of Korea. 3Department of Biology, University of Naples “Federico II”, Complesso Universitario Di Monte S. Angelo, Via Cupa Nuova Cinthia 21, 80126 Naples, Italy. 4Department of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, AB T2N 1N4, Canada. 5Biological and Genetic Resources Assessment Division, National Institute of Biological Resources, 42 Hwangyeong-ro, Seo-gu, Incheon 22689, Republic of Korea. 6Department of Biological Sciences and Research Center of Ecomimetics, College of Natural Sciences, Chonnam National University, Yongbong-ro, Buk-gu, Gwangju 61186, Republic of Korea.
Short-chain alkanes (SCA; C2-C4) emitted from geological sources contribute to photochemical pollution and ozone production in the atmosphere. Microorganisms that oxidize SCA and thereby mitigate their release from geothermal environments have rarely been studied. In this study, propane-oxidizing cultures could not be grown from acidic geothermal samples by enrichment on propane alone, but instead required methane addition, indicating that propane was co-oxidized by methanotrophs. “Methylacidiphilum” isolates from these enrichments did not grow on propane as a sole energy source but unexpectedly did grow on C3 compounds such as 2-propanol, acetone, and acetol. A gene cluster encoding the pathway of 2-propanol oxidation to pyruvate via acetol was upregulated during growth on 2-propanol. Surprisingly, this cluster included one of three genomic operons (pmoCAB3) encoding particulate methane monooxygenase (PMO), and several physiological tests indicated that the encoded PMO3 enzyme mediates the oxidation of acetone to acetol. Acetone-grown resting cells oxidized acetone and butanone but not methane or propane, implicating a strict substrate specificity of PMO3 to ketones instead of alkanes. Another PMO-encoding operon, pmoCAB2, was induced only in methane-grown cells, and the encoded PMO2 could be responsible for co-metabolic oxidation of propane to 2-propanol. In nature, propane probably serves primarily as a supplemental growth substrate for these bacteria when growing on methane.