Comparative genomics analyses indicate differential methylated amine utilization trait within members of the genus Gemmobacter.
Journal
Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
08
09
2020
revised:
11
01
2021
accepted:
11
01
2021
pubmed:
24
1
2021
medline:
5
4
2022
entrez:
23
1
2021
Statut:
ppublish
Résumé
Methylated amines are ubiquitous in the environment and play a role in regulating the earth's climate via a set of complex biological and chemical reactions. Microbial degradation of these compounds is thought to be a major sink. Recently we isolated a facultative methylotroph, Gemmobacter sp. LW-1, an isolate from the unique environment Movile Cave, Romania, which is capable of methylated amine utilization as a carbon source. Here, using a comparative genomics approach, we investigate how widespread methylated amine utilization is within members of the bacterial genus Gemmobacter. Seven genomes of different Gemmobacter species isolated from diverse environments, such as activated sludge, fresh water, sulphuric cave waters (Movile Cave) and the marine environment were available from the public repositories and used for the analysis. Our results indicate that methylamine utilization is a distinctive feature of selected members of the genus Gemmobacter, namely G. aquatilis, G. lutimaris, G. sp. HYN0069, G. caeni and G. sp. LW-1 have the genetic potential while others (G. megaterium and G. nectariphilus) have not.
Identifiants
pubmed: 33484104
doi: 10.1111/1758-2229.12927
doi:
Substances chimiques
Amines
0
DNA, Bacterial
0
Fatty Acids
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
195-208Informations de copyright
© 2021 The Authors. Environmental Microbiology Reports published by Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
Anthony, C. (1982) The Biochemistry of Methylotrophs. London: Academic Press.
Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., et al. (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
Baek, M.-G., Shin, S.-K., and Yi, H. (2020) Gemmobacter aquarius sp. nov., Runella rosea sp. nov. and Flavobacterium fluviale sp. nov., isolated from the Namhangang River system. Int J Syst Evol Microbiol: ijsem004455 70(11), 5640-5647.
Blom, J., Albaum, S.P., Doppmeier, D., Pühler, A., Vorhölter, F.-J., Zakrzewski, M., and Goesmann, A. (2009) EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinform 10: 154.
Burke, S.A., Lo, S.L., and Krzycki, J.A. (1998) Clustered genes encoding the methyltransferases of methanogenesis from monomethylamine. J Bacteriol 180: 3432-3440.
Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
Carpenter, L.J., Archer, S.D., and Beale, R. (2012) Ocean-atmosphere trace gas exchange. Chem Soc Rev 41: 6473-6506.
Chaumeil, P.A., Mussig, A.J., Hugenholtz, P., and Parks, D.H. (2019) GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36(6), 1925-1927.
Chen, W.M., Cho, N.T., Huang, W.C., Young, C.C., and Sheu, S.Y. (2013) Description of Gemmobacter fontiphilus sp nov., isolated from a freshwater spring, reclassification of Catellibacterium nectariphilum as Gemmobacter nectariphilus comb. nov., Catellibacterium changlense as Gemmobacter changlensis comb. nov., Catellibacterium aquatile as Gemmobacter aquaticus nom. nov., Catellibacterium caeni as Gemmobacter caeni comb. nov., Catellibacterium nanjingense as Gemmobacter nanjingensis comb. nov., and emended description of the genus Gemmobacter and of Gemmobacter aquatilis. Int J Syst Evol Microbiol 63: 470-478.
Chen, Y. (2012) Comparative genomics of methylated amine utilization by marine Roseobacter clade bacteria and development of functional gene markers (tmm, gmaS). Environ Microbiol 14: 2308-2322.
Chen, Y., McAleer, K.L., and Murrell, J.C. (2010a) Monomethylamine as a nitrogen source for a nonmethylotrophic bacterium, Agrobacterium tumefaciens. Appl Environ Microbiol 76: 4102-4104.
Chen, Y., Scanlan, J., Song, L., Crombie, A., Rahman, M.T., Schäfer, H., and Murrell, J.C. (2010b) γ-Glutamylmethylamide is an essential intermediate in the metabolism of methylamine by Methylocella silvestris. Appl Environ Microbiol 76: 4530-4537.
Chen, Y., Wu, L., Boden, R., Hillebrand, A., Kumaresan, D., Moussard, H., et al. (2009) Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile cave. ISME J 3: 1093-1104.
Chistoserdova, A.Y., Christoserdova, L.V., McIntire, W.S., and Lidstrom, M.E. (1994) Genetic organization of the mau gene cluster in Methylobacterium extorquens AM1: complete nucleotide sequence and generation and characteristics of mau mutants. J Bacteriol 176: 4052-4065.
Chistoserdova, L. (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13: 2603-2622.
Chistoserdova, L., Kalyuzhnaya, M.G., and Lidstrom, M.E. (2009) The expanding world of Methylotrophic metabolism. Annu Rev Microbiol 63: 477-499.
Eddy, S.R. (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195.
Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5: 113.
Emms, D.M., and Kelly, S. (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16: 157.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
Ge, X., Wexler, A.S., and Clegg, S.L. (2011) Atmospheric amines - part I. a review. Atmos Environ 45: 524-546.
Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P., and Tiedje, J.M. (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81-91.
Grant, J.R., Arantes, A.S., and Stothard, P. (2012) Comparing thousands of circular genomes using the CGView comparison tool. BMC Genomics 13: 202.
Hameed, A., Shahina, M., Lin, S.-Y., Chen, W.-M., Hsu, Y.-H., Lai, W.-A., and Young, C.-C. (2020) Description of Gemmobacter aestuarii sp. nov., isolated from estuarine surface water and reclassification of Cereibacter changlensis as Gemmobacter changlensis. Arch Microbiol, 202(5), 1035-1042.
Jones, D.T., Taylor, W.R., and Thornton, J.M. (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8: 275-282.
Kämpfer, P., Jerzak, L., Wilharm, G., Golke, J., Busse, H.-J., and Glaeser, S.P. (2015) Gemmobacter intermedius sp. nov., isolated from a white stork (Ciconia ciconia). Int J Syst Evol Microbiol 65: 778-783.
Kang, J.Y., Kim, M.-J., Chun, J., Son, K.P., and Jahng, K.Y. (2017) Gemmobacter straminiformis sp. nov., isolated from an artificial fountain. Int J Syst Evol Microbiol 67: 5019-5025.
Kim, M., Oh, H.-S., Park, S.-C., and Chun, J. (2014) Towards a taxonomic coherence between average nucleotide identity and 16S gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64: 346-351.
Konstantinidis, K.T., and Tiedje, J.M. (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102: 2567-2572.
Kumar, S., Stecher, G., and Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874.
Kumaresan, D., Stephenson, J., Doxey, A.C., Bandukwala, H., Brooks, E., Hillebrand-Voiculescu, A., et al. (2018) Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses. Microbiome 6: 1.
Kumaresan, D., Wischer, D., Hillebrand-Voiculescu, A.M., and Murrell, J.C. (2015) Draft genome sequences of facultative Methylotrophs, Gemmobacter sp. strain LW1 and Mesorhizobium sp. strain 1M-11, isolated from Movile cave, Romania. Genome Announc 3(6), e01266-15.
Kumaresan, D., Wischer, D., Stephenson, J., Hillebrand-Voiculescu, A., and Murrell, J.C. (2014) Microbiology of Movile cave - a chemolithoautotrophic ecosystem. Geomicrobiol J 31: 186-193.
Lagesen, K., Hallin, P., Rødland, E.A., Staerfeldt, H.-H., Rognes, T., and Ussery, D.W. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100-3108.
Latypova, E., Yang, S., Wang, Y.S., Wang, T., Chavkin, T.A., Hackett, M., et al. (2010) Genetics of the glutamate-mediated methylamine utilization pathway in the facultative methylotrophic beta-proteobacterium Methyloversatilis universalis FAM5. Mol Microbiol 75: 426-439.
Lee, M.D. (2019) GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 35: 4162-4164.
Lex, A., Gehlenborg, N., Strobelt, H., Vuillemot, R., and Pfister, H. (2014) UpSet: visualization of intersecting sets. IEEE Trans Vis Comput Graph 20: 1983-1992.
Lidbury, I., Kimberley, G., Scanlan, D.J., Murrell, J.C., and Chen, Y. (2015a) Comparative genomics and mutagenesis analyses of choline metabolism in the marine Roseobacter clade. Environ Microbiol 17: 5048-5062.
Lidbury, I., Mausz, M.A., Scanlan, D.J., and Chen, Y. (2017) Identification of dimethylamine monooxygenase in marine bacteria reveals a metabolic bottleneck in the methylated amine degradation pathway. ISME J 11: 1592-1601.
Lidbury, I., Murrell, J.C., and Chen, Y. (2014) Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria. Proc Natl Acad Sci 111: 2710-2715.
Lidbury, I.D., Murrell, J.C., and Chen, Y. (2015b) Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling. ISME J 9: 760-769.
Lidstrom, M.E. (2006) Aerobic Methylotrophic prokaryotes. In The Prokaryotes: Volume 2: Ecophysiology and Biochemistry. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E. (eds). New York, NY: Springer, pp. 618-634.
Lim, K., Kannan, A.D., Shobnam, N., Mahmood, M., Lee, J., and Im, J. (2020) Gemmobacter serpentinus sp. nov., isolated from conserved forages. Int J Syst Evol Microbiol 70: 4224-4232.
Liu, J.-J., Zhang, X.-Q., Chi, F.-T., Pan, J., Sun, C., and Wu, M. (2014) Gemmobacter megaterium sp. nov., isolated from coastal planktonic seaweeds. Int J Syst Evol Microbiol 64: 66-71.
Liu, Y., and Whitman, W.B. (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125: 171-189.
Liu, Y., Xu, C.-J., Jiang, J.-T., Liu, Y.-H., Song, X.-F., Li, H., and Liu, Z.-P. (2010) Catellibacterium aquatile sp. nov., isolated from fresh water, and emended description of the genus Catellibacterium Tanaka et al. 2004. Int J Syst Evol Microbiol 60: 2027-2031.
Lyimo, T.J., Pol, A., Jetten, M.S.M., and Op den Camp, H.J.M. (2009) Diversity of methanogenic archaea in a mangrove sediment and isolation of a new Methanococcoides strain. FEMS Microbiol Lett 291: 247-253.
Markowitz, V.M., Chen, I.-M.A., Palaniappan, K., Chu, K., Szeto, E., Pillay, M., et al. (2013) IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 42: D560-D567.
Matias Rodrigues, J.F., Schmidt, T.S.B., Tackmann, J., and von Mering, C. (2017) MAPseq: highly efficient k-mer search with confidence estimates, for rRNA sequence analysis. Bioinformatics 33: 3808-3810.
McIntire, W.S., Wemmer, D.E., Chistoserdova, A., and Lidstrom, M.E. (1991) A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase. Science 252: 817-824.
Nayak, D.D., Agashe, D., Lee, M.-C., and Marx, C.J. (2016) Selection maintains apparentlydegenerate metabolic pathwaysdueto tradeoffsin using methylamine for carbon versus nitrogen. Curr Biol 26: 1-11.
Nayak, D.D., and Marx, C.J. (2015) Experimental horizontal gene transfer of methylamine dehydrogenase mimics prevalent exchange in nature and overcomes the methylamine growth constraints posed by the sub-optimal N-Methylglutamate pathway. Microorganisms 3: 60-79.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., and Tyson, G.W. (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res: gr. 186072.186114. 25(7), 1043-1055.
Paul, L., Ferguson, D.J., and Krzycki, J.A. (2000) The trimethylamine methyltransferase gene and multiple dimethylamine methyltransferase genes of Methanosarcina barkeri contain in-frame and read-through amber codons. J Bacteriol 182: 2520-2529.
Price, M.N., Dehal, P.S., and Arkin, A.P. (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490.
Pruesse, E., Peplies, J., and Glöckner, F.O. (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
Qu, J.-H., Ma, W.-W., Zhou, J., Wang, X.-F., Lu, W.-L., Qu, L.-B., and Wang, L.-F. (2020) Gemmobacter caeruleus sp. nov., a novel species originating from lake sediment. Int J Syst Evol Microbiol 70: 1987-1992.
Richter, M., and Rossello-Mora, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126-19131.
Rodriguez-R, L.M., and Konstantinidis, K.T. (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints.
Rothe, B., Fischer, A., Hirsch, P., Sittig, M., and Stackebrandt, E. (1987) The phylogenetic position of the budding bacteria Blastobacter aggregatus and Gemmobacter aquatilis gen., nov. sp. nov. Arch Microbiol 147: 92-99.
Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
Schade, G.W., and Crutzen, P.J. (1995) Emission of aliphatic-amines from animal husbandry and their reactions - potential source of N2o and Hcn. J Atmos Chem 22: 319-346.
Sheu, S.-Y., Sheu, D.-S., Sheu, F.-S., and Chen, W.-M. (2013a) Gemmobacter tilapiae sp. nov., a poly-β-hydroxybutyrate-accumulating bacterium isolated from a freshwater pond. Int J Syst Evol Microbiol 63: 1550-1556.
Sheu, S.-Y., Shiau, Y.-W., Wei, Y.-T., and Chen, W.-M. (2013b) Gemmobacter lanyuensis sp. nov., isolated from a freshwater spring. Int J Syst Evol Microbiol 63: 4039-4045.
Tanaka, Y., Hanada, S., Manome, A., Tsuchida, T., Kurane, R., Nakamura, K., and Kamagata, Y. (2004) Catellibacterium nectariphilum gen. nov., sp. nov., which requires a diffusible compound from a strain related to the genus Sphingomonas for vigorous growth. Int J Syst Evol Microbiol 54: 955-959.
Taubert, M., Grob, C., Howat, A.M., Burns, O.J., Pratscher, J., Jehmlich, N., et al. (2017) Methylamine as a nitrogen source for microorganisms from a coastal marine environment. Environ Microbiol 19: 2246-2257.
Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
Wischer, D., Kumaresan, D., Johnston, A., El Khawand, M., Stephenson, J., Hillebrand-Voiculescu, A.M., et al. (2015) Bacterial metabolism of methylated amines and identification of novel methylotrophs in Movile Cave. ISME J 9: 195-206.
Yoo, Y., Lee, D.W., Lee, H., Kwon, B.-O., Khim, J.S., Yim, U.H., et al. (2019) Gemmobacter lutimaris sp. nov., a marine bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 69: 1676-1681.
Zhang, J., Chen, S.-A., Zheng, J.-W., Cai, S., Hang, B.-J., He, J., and Li, S.-P. (2012) Catellibacterium nanjingense sp. nov., a propanil-degrading bacterium isolated from activated sludge, and emended description of the genus Catellibacterium. Int J Syst Evol Microbiol 62: 495-499.
Zheng, J.-W., Chen, Y.-G., Zhang, J., Ni, Y.-Y., Li, W.-J., He, J., and Li, S.-P. (2011) Description of Catellibacterium caeni sp. now., reclassification of Rhodobacter changlensis Anil Kumar et al. 2007 as Catellibacterium changlense comb. nov. and emended description of the genus Catellibacterium. Int J Syst Evol Microbiol 61: 1921-1926.