Selection Maintains Apparently Degenerate Metabolic Pathways due to Tradeoffs in Using Methylamine for Carbon versus Nitrogen

Current Biology

Volumn 26, Issue 11, 2016, Pages 1416-1426

  Nayak, Dipti D ^a,c   Agashe, Deepa ^a,d   Lee, Ming Chun ^a,e   Marx, Christopher J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

experimental evolution; functional degeneracy; methylamine; Methylobacterium; methylotrophy

Indexed keywords

AMINE DEHYDROGENASE; BACTERIAL PROTEIN; CARBON; METHYLAMINE; NITROGEN; OXIDOREDUCTASE;

GENETIC SELECTION; GENETICS; METABOLISM; METHYLOBACTERIUM EXTORQUENS;

BACTERIAL PROTEINS; CARBON; METABOLIC NETWORKS AND PATHWAYS; METHYLAMINES; METHYLOBACTERIUM EXTORQUENS; NITROGEN; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; SELECTION, GENETIC;

EID: 84975488686     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.04.029     Document Type: Article

References (51)

1. 1 Marx, C.J., Miller, J.A., Chistoserdova, L., Lidstrom, M.E., Multiple formaldehyde oxidation/detoxification pathways in Burkholderia fungorum LB400. J. Bacteriol. 186 (2004), 2173–2178.
2. 2 Marx, C.J., Van Dien, S.J., Lidstrom, M.E., Flux analysis uncovers key role of functional redundancy in formaldehyde metabolism. PLoS Biol., 3, 2005, e16.
3. 3 Denef, V.J., Klappenbach, J.A., Patrauchan, M.A., Florizone, C., Rodrigues, J.L.M., Tsoi, T.V., Verstraete, W., Eltis, L.D., Tiedje, J.M., Genetic and genomic insights into the role of benzoate-catabolic pathway redundancy in Burkholderia xenovorans LB400. Appl. Environ. Microbiol. 72 (2006), 585–595.
4. 4 Gerth, M.L., Ferla, M.P., Rainey, P.B., The origin and ecological significance of multiple branches for histidine utilization in Pseudomonas aeruginosa PAO1. Environ. Microbiol. 14 (2012), 1929–1940.
5. 5 Tononi, G., Sporns, O., Edelman, G.M., Measures of degeneracy and redundancy in biological networks. Proc. Natl. Acad. Sci. USA 96 (1999), 3257–3262.
6. 6 Boucher, Y., Douady, C.J., Papke, R.T., Walsh, D.A., Boudreau, M.E.R., Nesbø, C.L., Case, R.J., Doolittle, W.F., Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37 (2003), 283–328.
7. 7 Kafri, R., Springer, M., Pilpel, Y., Genetic redundancy: new tricks for old genes. Cell 136 (2009), 389–392.
8. 8 Wang, Z., Zhang, J., Abundant indispensable redundancies in cellular metabolic networks. Genome Biol. Evol. 1 (2009), 23–33.
9. 9 Stelling, J., Sauer, U., Szallasi, Z., Doyle, F.J. 3rd, Doyle, J., Robustness of cellular functions. Cell 118 (2004), 675–685.
10. 10 van Heeswijk, W.C., Westerhoff, H.V., Boogerd, F.C., Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective. Microbiol. Mol. Biol. Rev. 77 (2013), 628–695.
11. 11 Helling, R.B., Speed versus efficiency in microbial growth and the role of parallel pathways. J. Bacteriol. 184 (2002), 1041–1045.
12. 12 Brenchley, J.E., Prival, M.J., Magasanik, B., Regulation of the synthesis of enzymes responsible for glutamate formation in Klebsiella aerogenes. J. Biol. Chem. 248 (1973), 6122–6128.
13. 13 Chistoserdova, L., Chen, S.W., Lapidus, A., Lidstrom, M.E., Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J. Bacteriol. 185 (2003), 2980–2987.
14. 14 Chistoserdova, L., Modularity of methylotrophy, revisited. Environ. Microbiol. 13 (2011), 2603–2622.
15. 1 assimilation and dissimilation pathways. J. Bacteriol. 196 (2014), 4130–4139.
16. 16 McIntire, W.S., Wemmer, D.E., Chistoserdov, A., Lidstrom, M.E., A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase. Science 252 (1991), 817–824.
17. 17 Chistoserdov, A.Y., Chistoserdova, L.V., McIntire, W.S., Lidstrom, M.E., Genetic organization of the mau gene cluster in Methylobacterium extorquens AM1: complete nucleotide sequence and generation and characteristics of mau mutants. J. Bacteriol. 176 (1994), 4052–4065.
18. 18 Chen, L., Durley, R.C., Mathews, F.S., Davidson, V.L., Structure of an electron transfer complex: methylamine dehydrogenase, amicyanin, and cytochrome c551i. Science 264 (1994), 86–90.
19. 19 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. 75 (2010), 426–439.
20. 20 Marx, C.J., Chistoserdova, L., Lidstrom, M.E., Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J. Bacteriol. 185 (2003), 7160–7168.
21. 21 Chistoserdova, L., Laukel, M., Portais, J.C., Vorholt, J.A., Lidstrom, M.E., Multiple formate dehydrogenase enzymes in the facultative methylotroph Methylobacterium extorquens AM1 are dispensable for growth on methanol. J. Bacteriol. 186 (2004), 22–28.
22. 22 Chistoserdova, L., Crowther, G.J., Vorholt, J.A., Skovran, E., Portais, J.-C., Lidstrom, M.E., Identification of a fourth formate dehydrogenase in Methylobacterium extorquens AM1 and confirmation of the essential role of formate oxidation in methylotrophy. J. Bacteriol. 189 (2007), 9076–9081.
23. 23 Crowther, G.J., Kosály, G., Lidstrom, M.E., Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J. Bacteriol. 190 (2008), 5057–5062.
24. 24 Nayak, D.D., Marx, C.J., 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 (2015), 60–79.
25. 25 Lee, M.C., Marx, C.J., Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet., 8, 2012, e1002651.
26. 26 Agashe, D., Martinez-Gomez, N.C., Drummond, D.A., Marx, C.J., Good codons, bad transcript: large reductions in gene expression and fitness arising from synonymous mutations in a key enzyme. Mol. Biol. Evol. 30 (2013), 549–560.
27. 27 Lee, M.C., Chou, H.H., Marx, C.J., Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63 (2009), 2816–2830.
28. 28 Agashe, D., Sane, M., Phalnikar, K., Diwan, G.D., Habibullah, A., Martinez-Gomez, N.C., Sahasrabuddhe, V., Polachek, W., Wang, J., Chubiz, L.M., Marx, C.J., Large-effect beneficial synonymous mutations mediate rapid and parallel adaptation in a bacterium. Mol. Biol. Evol. 33 (2016), 1542–1553.
29. 29 Vorholt, J.A., Marx, C.J., Lidstrom, M.E., Thauer, R.K., Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J. Bacteriol. 182 (2000), 6645–6650.
30. 30 Barrick, J.E., Corbino, K.A., Winkler, W.C., Nahvi, A., Mandal, M., Collins, J., Lee, M., Roth, A., Sudarsan, N., Jona, I., et al. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc. Natl. Acad. Sci. USA 101 (2004), 6421–6426.
31. 31 Ferguson, G.P., Nikolaev, Y., McLaggan, D., Maclean, M., Booth, I.R., Survival during exposure to the electrophilic reagent N-ethylmaleimide in Escherichia coli: role of KefB and KefC potassium channels. J. Bacteriol. 179 (1997), 1007–1012.
32. 32 Rasche, M.E., Havemann, S.A., Rosenzvaig, M., Characterization of two methanopterin biosynthesis mutants of Methylobacterium extorquens AM1 by use of a tetrahydromethanopterin bioassay. J. Bacteriol. 186 (2004), 1565–1570.
33. 4) metabolism. Biotechnol. Bioeng. 78 (2002), 296–312.
34. 34 Chou, H.H., Marx, C.J., Optimization of gene expression through divergent mutational paths. Cell Rep. 1 (2012), 133–140.
35. 35 Michener, J.K., Camargo Neves, A.A., Vuilleumier, S., Bringel, F., Marx, C.J., Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post-transfer refinement. eLife 3 (2014), 1–16.
36. + channels and transporters by controlling the dimer-hinge conformation. Structure 17 (2009), 893–903.
37. 37 Carroll, S.M., Chubiz, L.M., Agashe, D., Marx, C.J., Parallel and divergent evolutionary solutions for the optimization of an engineered central metabolism in Methylobacterium extorquens AM1. Microorganisms 3 (2015), 152–174.
38. 38 Martinez-Gomez, N.C., Nguyen, S., Lidstrom, M.E., Elucidation of the role of the methylene-tetrahydromethanopterin dehydrogenase MtdA in the tetrahydromethanopterin-dependent oxidation pathway in Methylobacterium extorquens AM1. J. Bacteriol. 195 (2013), 2359–2367.
39. 39 Singer, M.A., Do mammals, birds, reptiles and fish have similar nitrogen conserving systems?. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 134 (2003), 543–558.
40. 40 Weeks, D.L., Eskandari, S., Scott, D.R., Sachs, G., A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287 (2000), 482–485.
41. 41 Tegos, G.P., Masago, K., Aziz, F., Higginbotham, A., Stermitz, F.R., Hamblin, M.R., Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation. Antimicrob. Agents Chemother. 52 (2008), 3202–3209.
42. 42 Padan, E., Bibi, E., Ito, M., Krulwich, T.A., Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717 (2005), 67–88.
43. 43 Ge, X., Wexler, A.S., Clegg, S.L., Atmospheric amines - Part I. A review. Atmos. Environ. 45 (2011), 524–546.
44. 44 Nayak, D.D., Marx, C.J., Genetic and phenotypic comparison of facultative methylotrophy between Methylobacterium extorquens strains PA1 and AM1. PLoS ONE, 9, 2014, e107887.
45. 45 Delaney, N.F., Kaczmarek, M.E., Ward, L.M., Swanson, P.K., Lee, M.C., Marx, C.J., Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. PLoS ONE, 8, 2013, e62957.
46. 46 Marx, C.J., Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res. Notes, 1, 2008, 1.
47. 47 Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C.A. 3rd, Smith, H.O., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6 (2009), 343–345.
48. 48 Nash, T., The colorimetric estimation of formaldehyde by means of the Hantzsch reaction. Biochem. J. 55 (1953), 416–421.
49. 1 compounds from natural and industrial sources. PLoS ONE, 4, 2009, e5584.
50. 50 Barrick, J.E., Colburn, G., Deatherage, D.E., Traverse, C.C., Strand, M.D., Borges, J.J., Knoester, D.B., Reba, A., Meyer, A.G., Identifying structural variation in haploid microbial genomes from short-read resequencing data using breseq. BMC Genomics, 15, 2014, 1039.
51. 51 Chou, H.H., Berthet, J., Marx, C.J., Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet., 5, 2009, e1000652.