Abstract
Over the past two decades, application of high-throughput technologies for molecular analysis, collectively referred to as omics , have revolutionized the field of biology . These technologies enable collecting large amounts of data on DNA and RNA sequences, protein and metabolite identities, which can then be incorporated into metabolic models that can simulate metabolisms. Omics have been applied to studying methanotrophy for a long time, and progress in this area has been summarised previously, including recent reviews. In this chapter, we only highlight the very latest novel insights into methanotrophy through omics . Some of the highlights are the newly uncovered environmental dominance of the Methylobacter species , the discovery of novel methanotroph taxa through metagenome -assembled genome reconstruction, further insights into the role of lanthanides in methanotrophy, and further details on detection of the presence and activities of different guilds of methanotrophs across geochemical gradients . We also touch briefly on the novel developments in understanding of the communal function in methanotrophy, and on the role of model organisms in further advancements of our knowledge.
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References
Akberdin IR, Thompson M, Hamilton R, Desai N, Alexander D, Henard CA, Guarnieri MT, Kalyuzhnaya MG (2018a) Methane utilization in Methylomicrobium alcaliphilum 20ZR: a systems approach. Sci Rep 8:2512
Akberdin IR, Collins DA, Hamilton R, Oshchepkov DY, Shukla AK, Nicora CD, Nakayasu ES, Adkins JN, Kalyuzhnaya MG (2018b) Rare earth elements alter redox balance in Methylomicrobium alcaliphilum 20ZR. Front Microbiol 9:2735
Arora-Williams K, Olesen SW, Scandella B, Delwich K, Spencer SJ, Myers E, Abraham S, Sooklal A, Preheim SP (2018) Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake. Microbiome 6:165
Auman AJ, Stolyar S, Costello AM, Lidstrom ME (2000) Molecular characterization of methanotrophic isolates from freshwater lake sediment. Appl Environ Microbiol 66:5259–5266
Beck DA, Kalyuzhnaya MG, Malfatti S, Tringe SG, Glavina del Rio T, Ivanova N, Lidstrom ME, Chistoserdova L (2013) A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae. Peer J 1:e23
Beck DA, McTaggart TL, Setboonsarng U, Vorobev A, Kalyuzhnaya MG, Ivanova N, Goodwin L, Woyke T, Lidstrom ME, Chistoserdova L (2014) The expanded diversity of Methylophilaceae from Lake Washington through cultivation and genomic sequencing of novel ecotypes. PLoS One 9:e102458
Biderre-Petit C, Taib N, Gardon H, Hochart C, Debroas D (2018) New insights into the pelagic microorganisms involved in the methane cycle in the meromictic Lake Pavin through metagenomics. FEMS Microbiol Ecol 95(3):fiy183. https://doi.org/10.1093/femsec/fiy183
Butterfield CN, Li Z, Andeer PF, Spaulding S, Thomas BC, Singh A, Hettich RL, Suttle KB, Probst AJ, Tringe SG, Northen T, Pan C, Banfield JF (2016) Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone. Peer J 4:e2687
Case DH, Ijiri A, Morono Y, Tavormina P, Orphan VJ, Inagaki F (2017) Aerobic and anaerobic methanotrophic communities associated with methane hydrates exposed on the seafloor: a high-pressure sampling and stable isotope-incubation experiment. Front Microbiol 8:2569
Chistoserdova L (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13:2603–2622
Chistoserdova L (2015) Methylotrophs in natural habitats: current insights through metagenomics. Appl Microbiol Biotechol 99:5763–5779
Chistoserdova L (2016) Lanthanides: new life metals? World J Microbiol Biotechnol 32:138
Chistoserdova L (2017) Omics approaches to studying methylotrophs and methylotroph communities. Curr Issues Mol Biol 24:119–142
Chistoserdova L (2019) New pieces to the lanthanide puzzle. Mol Microbiol 111(5):1127–1131. https://doi.org/10.1111/mmi.14210
Chistoserdova L, Kalyuzhnaya MG (2018) Current trends in methylotrophy. Trends Microbiol 26:703–714
Chistoserdova L, Lidstrom ME (2013) Aerobic methylotrophic prokaryotes. In: Rosenberg E, EF DL, Thompson F, Lory S, Stackebrandt E (eds) The prokaryotes, 4th edn. Springer, Berlin, pp 267–285
Chu F, Lidstrom ME (2016) XoxF acts as the predominant methanol dehydrogenase in the Type I methanotroph Methylomicrobium buryatense. J Bacteriol 198:1317–1325
Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292
de la Torre A, Metivier A, Chu F, Laurens LM, Beck DA, Pienkos PT, Lidstrom ME, Kalyuzhnaya MG (2015) Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1). Microb Cell Factories 14:188
Deng Y, Gui Q, Dumont M, Han C, Deng H, Yun J, Zhong W (2019) Methylococcaceae are the dominant active aerobic methanotrophs in a Chinese tidal marsh. Environ Sci Pollut Res Int 26:636–646
Edwards CR, Onstott TC, Miller JM, Wiggins JB, Wang W, Lee CK, Cary SC, Pointing SB, Lau MCY (2017) Draft genome sequence of uncultured upland soil cluster gammaproteobacteria gives molecular insights into high-affinity methanotrophy. Genome Announc 5:e00047-17
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548
Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, Tyson GW (2019) An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol 17:219–232. https://doi.org/10.1038/s41579-018-0136-7
Gilman A, Fu Y, Hendershott M, Chu F, Puri AW, Smith AL, Pesesky M, Lieberman R, Beck DAC, Lidstrom ME (2017) Oxygen-limited metabolism in the methanotroph Methylomicrobium buryatense 5GB1C. Peer J 5:e3945
Guerrero-Cruz S, Cremers G, van Alen TA, Op den Camp HJM, MSM J, Rasigraf O, Vaksmaa A (2018) Response of the anaerobic methanotroph “Candidatus Methanoperedens nitroreducens” to oxygen stress. Appl Environ Microbiol 84:e01832-18
Hernandez ME, Beck DA, Lidstrom ME, Chistoserdova L (2015) Oxygen availability is a major factor in determining the composition of microbial communities involved in methane oxidation. Peer J 3:e801
Kalyuzhnaya MG, Lapidus A, Ivanova N, Copeland AC, McHardy AC, Szeto E, Salamov A, Grigoriev IV, Suciu D, Levine SR, Markowitz VM, Rigoutsos I, Tringe SG, Bruce DC, Richardson PM, Lidstrom ME, Chistoserdova L (2008) High-resolution metagenomics targets specific functional types in complex microbial communities. Nat Biotechnol 26:1029–1034
Kalyuzhnaya MG, Yang S, Rozova ON, Smalley NE, Clubb J, Lamb A, Gowda GA, Raftery D, Fu Y, Bringel F, Vuilleumier S, Beck DA, Trotsenko YA, Khmelenina VN, Lidstrom ME (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785
Kalyuzhnaya MG, Lamb AE, McTaggart TL, Oshkin IY, Shapiro N, Woyke T, Chistoserdova L (2015) Draft genomes of gammaproteobacterial methanotrophs isolated from Lake Washington sediment. Genome Announc 3:e00103–15
Karl DM, Beversdorf L, Björkman KM, Church MJ, Martinez A, DeLong EF (2008) Aerobic production of methane in the sea. Nat Geosci 1:473–478
Keppler F, Hamilton JTG, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191
Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334
Krause SMB, Johnson T, Samadhi Karunaratne Y, Fu Y, Beck DAC, Chistoserdova L, Lidstrom ME (2017) Lanthanide-dependent cross-feeding of methane derived carbon is linked by microbial community interactions. Proc Natl Acad Sci U S A 114:358–363
Lieven C, Petersen LAH, Jørgensen SB, Gernaey KV, Herrgard MJ, Sonnenschein N (2018) A genome-scale metabolic odel for Methylococcus capsulatus (Bath) suggests reduced efficiency electron transfer to the particulate methane onooxygenase. Front Microbiol 9:2947
Martinez-Cruz K, Leewis MC, Herriott IC, Sepulveda-Jauregui A, Anthony KW, Thalasso F, Leigh MB (2017) Anaerobic oxidation of methane by aerobic methanotrophs in sub-Arctic lake sediments. Sci Total Environ 607–608:23–31
Martinez-Cruz K, Sepulveda-Jauregui A, Casper P, Anthony KW, Smemo KA, Thalasso F (2018) Ubiquitous and significant anaerobic oxidation of methane in freshwater lake sediments. Water Res 144:332–340
McTaggart TL, Benuska G, Shapiro N, Woyke T, Chistoserdova L (2015) Draft genomes of five new strains of Methylophilaceae isolated from Lake Washington sediment. Genome Announc 3:e01511-14
Modin O, Fukushi K, Yamamoto K (2007) Denitrification with methane as external carbon source. Water Res 41:2726–2738
Murrell JC, McGovan V, Cardy DLN (1993) Detection of methylotrophic bacteria in natural samples by molecular probing techniques. Chemosphere 26:1–11
Ochsner AM, Hemmerle L, Vonderach T, Nüssli R, Bortfeld-Miller M, Hattendorf B, Vorholt JA (2019) Use of rare-earth elements in the phyllosphere colonizer Methylobacterium extorquens PA1. Mol Microbiol 111(5):1152–1166. https://doi.org/10.1111/mmi.14208
Oshkin IY, Beck DA, Lamb AE, Tchesnokova V, Benuska G, McTaggart TL, Kalyuzhnaya MG, Dedysh SN, Lidstrom ME, Chistoserdova L (2015) Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response. ISME J 9:1119–1129
Oswald K, Graf JS, Littmann S, Tienken D, Brand A, Wehrli B, Albertsen M, Daims H, Wagner M, Kuypers MM, Schubert CJ, Milucka J (2017) Crenothrix are major methane consumers in stratified lakes. ISME J 11:2124–2140
Padilla CC, Bertagnolli AD, Bristow LA, Sarode N, Glass JB, Thamdrup B, Stewart FJ (2017) Metagenomic binning recovers a transcriptionally active gammaproteobacterium linkinbg methanotrophy to partial denitrification in an anoxic oxygen minimum zone. Front Mar Sci 4:23
Paul BG, Ding H, Bagby SC, Kellermann MY, Redmond MC, Andersen GL, Valentine DL (2017) Methane-oxidizing bacteria shunt carbon to microbial mats at a marine hydrocarbon seep. Front Microbiol 8:186
Puri AW, Schaefer AL, Fu Y, Beck DA, Greenberg EP, Lidstrom ME (2017) Quorum sensing in a methane-oxidizing bacterium. J Bacteriol 199:e00773-16
Ruff SE, Arnds J, Knittel K, Amann R, Wegener G, Ramette A, Boetius A (2013) Microbial communities of deep-sea methane seeps at Hikurangi continental margin (New Zealand). PLoS One 8:e72627
Ruff SE, Felden J, Gruber-Vodicka HR, Marcon Y, Knittel K, Ramette A, Boetius A (2019) In situ development of a methanotrophic microbiome in deep-sea sediments. ISME J 13:197–213
Schütte UM, Cadieux SB, Hemmerich C, Pratt LM, White JR (2016) Unanticipated geochemical and microbial community structure under seasonal ice cover in a dilute, dimictic Arctic lake. Front Microbiol 7:1035
Sherwood Lollar B, Lacrampe-Couloumea G, Slatera GF, Warda J, Moserb DP, Gihringb TM, Linc L-H, Onstottc TC (2006) Unravelling abiogenic and biogenic sources of methane in the Earth’s deep subsurface. Chem Geol 226:328–339
Singleton CM, McCalley CK, Woodcroft BJ, Boyd JA, Evans PN, Hodgkins SB, Chanton JP, Frolking S, Crill PM, Saleska SR, Rich VI, Tyson GW (2018) Methanotrophy across a natural permafrost thaw environment. ISME J 12:2544–2558
Skennerton CT, Ward LM, Michel A, Metcalfe K, Valiente C, Mullin S, Chan KY, Gradinaru V, Orphan VJ (2015) Genomic reconstruction of an uncultured hydrothermal vent gammaproteobacterial methanotroph (family Methylothermaceae) indicates multiple adaptations to oxygen limitation. Front Microbiol 6:1425
Smith GJ, Angle JC, Solden LM, Borton MA, Morin TH, Daly RA, Johnston MD, Stefanik KC, Wolfe R, Gil B, Wrighton KC (2018) Members of the genus Methylobacter are inferred to account for the majority of aerobic methane oxidation in oxic soils from a freshwater wetland. MBio 9:e00815-18
Tanaka K, Yokoe S, Igarashi K, Takashino M, Ishikawa M, Hori K, Nakanishi S, Kato S (2018) Extracellular electron transfer via outer membrane cytochromes in a methanotrophic bacterium Methylococcus capsulatus (Bath). Front Microbiol 9:2905
Tindall BJ (2019) On the nomenclatural types of Methylothermus thermalis Tsubota et al. 2005, Methylothermus Tsubota et al. 2005 and Methylothermaceae Hirayama et al. 2014, their status under the International Code of Nomenclature of Prokaryotes and valid publication of the names Methylothermus gen. nov., Methylothermus subterraneus Hirayama et al. and Methylothermaceae Hirayama et al. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.003220
Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 6:183–229
Valentine DL, Reeburgh WS (2000) New perspectives on anaerobic methane oxidation. Environ Microbiol 2:477–484
Vekeman B, Speth D, Wille J, Cremers G, De Vos P, Op den Camp HJ, Heylen K (2016) Genome characteristics of two novel Type I methanotrophs enriched from North Sea sediments containing exclusively a lanthanide-dependent XoxF5-type methanol dehydrogenase. Microb Ecol 72:503–509
Versantvoort W, Guerrero-Cruz S, Speth DR, Frank J, Gambelli L, Cremers G, van Alen T, Jetten MSM, Kartal B, Op den Camp HJM, Reimann J (2018) Comparative genomics of Candidatus methylomirabilis species and description of Ca. Methylomirabilis lanthanidiphila. Front Microbiol 9:1672
Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang L, Scanlan D, Kang KH, Lewis M, Nelson KE, Methé B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren Q, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2:e303
Yan X, Chu F, Puri AW, Fu Y, Lidstrom ME (2016) Electroporation-based genetic manipulation in type I methanotrophs. Appl Environ Microbiol 82:2062–2069
Yu Z, Krause SM, Beck DA, Chistoserdova L (2016) A synthetic ecology perspective: how well does behavior of model organisms in the laboratory predict microbial activities in natural habitats? Front Microbiol 7:946
Yu Z, Beck DAC, Chistoserdova L (2017) Natural selection in synthetic communities highlights the roles of Methylococcaceae and Methylophilaceae and suggests differential roles for alternative methanol dehydrogenases in methane consumption. Front Microbiol 8:2392
Yu Z, Zheng Y, Huang J, Chistoserdova L (2019) Systems biology meets enzymology: recent insights into communal metabolism of methane and the role of lanthanides. Curr Issues Mol Biol 33:183–196
Zheng Y, Huang J, Zhao F, Chistoserdova L (2018) Physiological effect of XoxG(4) on lanthanide-dependent methanotrophy. mBio 9(2):e02430-17
Acknowledgements
This material is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC-0016224.
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Zheng, Y., Chistoserdova, L. (2019). Multi-omics Understanding of Methanotrophs. In: Lee, E. (eds) Methanotrophs. Microbiology Monographs, vol 32. Springer, Cham. https://doi.org/10.1007/978-3-030-23261-0_4
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