Genomics of methylotrophy in gram-positive methylamine-utilizing bacteria

Microorganisms

Volumn 3, Issue 1, 2015, Pages 94-112

  McTaggart, Tami L ^a   Beck, David A C ^a,b   Setboonsarng, Usanisa ^a   Shapiro, Nicole ^c   Woyke, Tanja ^c   Lidstrom, Mary E ^a,b   Kalyuzhnaya, Marina G ^b   Chistoserdova, Ludmila ^a  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

Arthrobacter; Bacillus; Genomics; Lake Washington; Methylotrophy; Mycobacterium

Indexed keywords

EID: 84932193023     PISSN: None     EISSN: 20762607     Source Type: Journal    
DOI: 10.3390/microorganisms3010094     Document Type: Article

References (42)

1. Anthony, C. The Biochemistry of Methylotrophs; Academic Press: London, UK, 1982.
2. Chistoserdova, L.; Lidstrom, M.E. Aerobic methylotrophic prokaryotes. In The Prokaryotes, 4th ed.; Rosenberg, E., DeLong, E.F., Thompson, F., Lory, S., Stackebrandt, E., Eds.; Springer: Berlin Heidelberg, Germany, 2013; pp. 267–285.
3. Ward, N.; Larsen, Ø.; Sakwa, J.; Bruseth, L.; Khouri, H.; Durkin, A.S.; Dimitrov, G.; Jiang, L.; Scanlan, D.; Kang, K.H.; et al. Genomic insights into methanotrophy: The complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol. 2004, 2, e303.
4. Hou, S.; Makarova, K.S.; Saw, J.H.; Senin, P.; Ly, B.V.; Zhou, Z.; Ren, Y.; Wang, J.; Galperin, M.Y.; Omelchenko, M.V.; et al. Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol. Direct 2008, 3, 26.
5. Khadem, A.F.; Wieczorek, A.S.; Pol, A.; Vuilleumier, S.; Harhangi, H.R.; Dunfield, P.F.; Kalyuzhnaya, M.G.; Murrell, J.C.; Francoijs, K.J.; Stunnenberg, H.G.; et al. Draft genome sequence of the volcano-inhabiting thermoacidophilic methanotroph Methylacidiphilum fumariolicum strain SolV. J. Bacteriol. 2012, 194, 3729–3730.
6. Ettwig, K.F.; Butler, M.K.; le Paslier, D.; Pelletier, E.; Mangenot, S.; Kuypers, M.M.; Schreiber, F.; Dutilh, B.E.; Zedelius, J.; de Beer, D.; et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 2010, 464, 543–548.
7. De Boer, L.; Brouwer, J.W.; van Hassel, C.W.; Levering, P.R.; Dijkhuizen, L. Nitrogen metabolism in the facultative methylotroph Arthrobacter P1 grown with various amines or ammonia as nitrogen sources. Antonie Van Leeuwenhoek 1989, 56, 221–232.
8. Vonck, J.; Arfman, N.; de Vries, G.E.; van Beeumen, J.; van Bruggen, E.F.; Dijkhuizen, L. Electron microscopic analysis and biochemical characterization of a novel methanol dehydrogenase from the thermotolerant Bacillus sp. C1. J. Biol. Chem. 1991, 266, 3949–3954.
9. De Vries, G.E.; Arfman, N.; Terpstra, P.; Dijkhuizen, L. Cloning, expression, and sequence analysis of the Bacillus methanolicus C1 methanol dehydrogenase gene. J. Bacteriol. 1992, 174, 5346–5353.
10. Zhang, X.; Fuller, J.H.; McIntire, W.S. Cloning, sequencing, expression, and regulation of the structural gene for the copper/topa quinone-containing methylamine oxidase from Arthrobacter strain P1, a Gram-positive facultative methylotroph. J. Bacteriol. 1993, 175, 5617–5627.
11. Bystrykh, L.V.; Vonck, J.; van Bruggen, E.F.; van Beeumen, J.; Samyn, B.; Govorukhina, N.I.; Arfman, N.; Duine, J.A.; Dijkhuizen, L. Electron microscopic analysis and structural characterization of novel NADP(H)-containing methanol: N,N′-dimethyl-4-nitrosoaniline oxidoreductases from the Gram-positive methylotrophic bacteria Amycolatopsis methanolica and Mycobacterium gastri MB19. J. Bacteriol. 1993, 175, 1814–1822.
12. Park, H.; Lee, H.; Ro, Y.T.; Kim, Y.M. Identification and functional characterization of a gene for the methanol: N,N′-dimethyl-4-nitrosoaniline oxidoreductase from Mycobacterium sp. strain JC1 (DSM 3803). Microbiology 2010, 156, 463–471.
13. Heggeset, T.M.; Krog, A.; Balzer, S.; Wentzel, A.; Ellingsen, T.E.; Brautaset, T. Genome sequence of thermotolerant Bacillus methanolicus: features and regulation related to methylotrophy and production of L-lysine and L-glutamate from methanol. Appl. Environ. Microbiol. 2012, 78, 5170–5181.
14. Irla, M.; Neshat, A.; Winkler, A.; Albersmeier, A.; Heggeset, T.M.; Brautaset, T.; Kalinowski, J.; Wendisch, V.F.; Rückert, C. Complete genome sequence of Bacillus methanolicus MGA3, a thermotolerant amino acid producing methylotroph. J. Biotechnol. 2014, 188C, 110–111.
15. Müller, J.E.; Heggeset, T.M.; Wendisch, V.F.; Vorholt, J.A.; Brautaset, T. Methylotrophy in the thermophilic Bacillus methanolicus, basic insights and application for commodity production from methanol. Appl. Microbiol. Biotechnol. 2015, 99, 535–551.
16. Colby, J.; Zatman, L.J. Enzymological aspects of the pathways for trimethylamine oxidation and C1 assimilation of obligate methylotrophs and restricted facultative methylotrophs. Biochem. J. 1975, 148, 513–520.
17. Boulton, C.A.; Large, P.J. Inactivation of trimethylamine N-oxide aldolase (demethylase) during preparation of bacterial extracts. FEMS Microbiol. Lett. 1979, 5, 159–162.
18. Chen, Y.; Patel, N.A.; Crombie, A.; Scrivens, J.H.; Murrell, J.C. Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase. Proc. Natl. Acad. Sci. USA 2011, 108, 17791–17796.
19. Kalyuzhnaya, M.G.; Lidstrom, M.E.; Chistoserdova, L. Utility of environmental probes targeting ancient enzymes: Methylotroph detection in Lake Washington. Microb. Ecol. 2004, 48, 436–472.
20. Beck, D.A.C.; McTaggart, T.L.; Setboonsarng, U.; Vorobev, A.; Kalyuzhnaya, M.G.; Ivanova, N.; Goodwin, L.; Woyke, T.; Lidstrom, M.E.; Chistoserdova, L. The expanded diversity of Methylophilaceae from Lake Washington through cultivation and genomic sequencing of novel ecotypes. PLoS One 2014, 9, e102458.
21. Beck, D.A.C.; McTaggart, T.L.; Setboonsarng, U.; Vorobev, A.; Kalyuzhnaya, M.G.; Goodwin, L.; Shapiro, N.; Woyke, T.; Lidstrom, M.E.; Chistoserdova, L. Multiphyletic origins of methylotrophy in Alphaproteobacteria, exemplified by comparative genomics of Lake Washington isolates. Environ. Microbiol. 2015, 17, 547–554.
22. Kalyuzhnaya, M.G.; Bowerman, S.; Lara, J.C.; Lidstrom, M.E.; Chistoserdova, L. Methylotenera mobilis gen. nov., sp. nov., an obligately methylamine-utilizing bacterium within the family Methylophilaceae. Int. J. Syst. Evol. Microbiol. 2006, 56, 2819–2823.
23. Chin, C.; Alexander, D.; Marks, P.; Klammer, A.; Drake, J.; Heiner, C.; Clum, A.; Copeland, A.; Huddleston, J.; Eichler, E.; et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 2013, 10, 563–569.
24. Gnerre, S.; MacCallum, I.; Przybylski, D.; Ribeiro, F.J.; Burton, J.N.; Walker, B.J.; Sharpe, T.; Hall, G.; Shea, T.P.; Sykes, S.; et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. USA 2011, 108, 1513–1518.
25. Zerbino, D.; Birney, E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008, 18, 821–829.
26. Hyatt, D.; Chen, G.L.; Lacascio, P.F.; Land, M.L.; Larimer, F.W.; Hauser, L.J. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010, 11, 119.
27. Pati, A.; Ivanova, N.N.; Mikhailova, N.; Ovchinnikova, G.; Hooper, S.D.; Lykidis, A.; Kyrpides, N.C. GenePRIMP: A gene prediction improvement pipeline for prokaryotic genomes. Nat. Methods 2010, 7, 455–457.
28. Lowe, T.M.; Eddy, S.R. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucl. Acids Res. 1997, 25, 955–964.
29. Pruesse, E.; Quast, C.; Knittel, K.; Fuchs, B.M.; Ludwig, W.; Peplies, J.; Glckner, F.O. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl. Acids Res. 2007, 35, 7188–7196.
30. INFERNAL. Inference of RNA Alignments. Available online: http://infernal.janelia.org (accessed on 1 April 2014).
31. Markowitz, V.M.; Chen, I.M.; Palaniappan, K.; Chu, K.; Szeto, E.; Pillay, M.; Ratner, A.; Huang, J.; Woyke, T.; Huntemann, M.; et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucl. Acids Res. 2014, 42, D560–D567.
32. Konstantinidis, K.T.; Tiedje, J.M. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 2005, 187, 6258–6264.
33. Summers, M.L.; Wallis, J.G.; Campbell, E.L.; Meeks, J.C. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J. Bacteriol. 1995, 177, 6184–6194.
34. Latypova, E.; Yang, S.; Wang, Y.S.; Wang, T.; Chavkin, T.A.; Hackett, M.; Schäfer, H.; Kalyuzhnaya, M.G. Genetics of the glutamate-mediated methylamine utilization pathway in the facultative methylotrophic beta-proteobacterium Methyloversatilis universalis FAM5. Mol. Microbiol. 2010, 75, 426–439.
35. Chen, Y.; Scanlan, J.; Song, L.; Crombie, A.; Rahman, M.T.; Schäfer, H.; Murrell, J.C. γ-glutamylmethylamide is an essential intermediate in the metabolism of methylamine by Methylocella silvestris. Appl. Environ. Microbiol. 2010, 76, 4530–4537.
36. Chen, Y.; McAleer, K.L.; Murrell, J.C. Monomethylamine as a nitrogen source for a nonmethylotrophic bacterium, Agrobacterium tumefaciens. Appl. Environ. Microbiol. 2010, 76, 4102–4104.
37. Parkin, K.L.; Hultinj, H.O. Characterization of trimethylamine-N-oxide (TMAO) demethylase activity from fish muscle microsomes. Biochemistry 1986, 100, 77–86.
38. Lidbury, I.; Murrell, J.C.; Chen, Y. Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria. Proc. Natl. Acad. Sci. USA 2014, 111, 2710–2740.
39. Chistoserdova, L. Modularity of methylotrophy, revisited. Environ. Microbiol. 2011, 13, 2603–2622.
40. Peyraud, R.; Schneider, K.; Kiefer, P.; Massou, S.; Vorholt, J.A.; Portais, J.C. Genome-scale reconstruction and system level investigation of the metabolic network of Methylobacterium extorquens AM1. BMC Syst. Biol. 2011, 5, 189.
41. Kalyuzhnaya, M.G.; Lidstrom, M.E. QscR-mediated transcriptional activation of serine cycle genes in Methylobacterium extorquens AM1. J. Bacteriol. 2005, 187, 7511–7517.
42. Kato, N.; Yurimoto, H.; Thauer, R.K. The physiological role of the ribulose monophosphate pathway in bacteria and archaea. Biosci. Biotechnol. Biochem. 2006, 70, 10–21.