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Microorganisms 2015, 3(1), 60-79; doi:10.3390/microorganisms3010060

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

1,2,†
and
1,2,3,4,*
1
Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
2
Biological Sciences, University of Idaho, Moscow, ID 83844, USA
3
Faculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA
4
Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID 83844, USA
Present Address: Institute for Genomic Biology, University of Illinois, Urbana, IL 61801, USA.
*
Author to whom correspondence should be addressed.
Academic Editor: Ludmila Chistoserdova
Received: 19 December 2014 / Revised: 16 February 2015 / Accepted: 16 February 2015 / Published: 10 March 2015
(This article belongs to the Special Issue Microbial C1 Metabolism)
View Full-Text   |   Download PDF [1019 KB, uploaded 10 March 2015]   |  

Abstract

Methylamine plays an important role in the global carbon and nitrogen budget; microorganisms that grow on reduced single carbon compounds, methylotrophs, serve as a major biological sink for methylamine in aerobic environments. Two non-orthologous, functionally degenerate routes for methylamine oxidation have been studied in methylotrophic Proteobacteria: Methylamine dehydrogenase and the N-methylglutamate pathway. Recent work suggests the N-methylglutamate (NMG) pathway may be more common in nature than the well-studied methylamine dehydrogenase (MaDH, encoded by the mau gene cluster). However, the distribution of these pathways across methylotrophs has never been analyzed. Furthermore, even though horizontal gene transfer (HGT) is commonly invoked as a means to transfer these pathways between strains, the physiological barriers to doing so have not been investigated. We found that the NMG pathway is both more abundant and more universally distributed across methylotrophic Proteobacteria compared to MaDH, which displays a patchy distribution and has clearly been transmitted by HGT even amongst very closely related strains. This trend was especially prominent in well-characterized strains of the Methylobacterium extroquens species, which also display significant phenotypic variability during methylamine growth. Strains like Methylobacterium extorquens PA1 that only encode the NMG pathway grew on methylamine at least five-fold slower than strains like Methylobacterium extorquens AM1 that also possess the mau gene cluster. By mimicking a HGT event through the introduction of the M. extorquens AM1 mau gene cluster into the PA1 genome, the resulting strain instantaneously achieved a 4.5-fold increase in growth rate on methylamine and a 11-fold increase in fitness on methylamine, which even surpassed the fitness of M. extorquens AM1. In contrast, when three replicate populations of wild type M. extorquens PA1 were evolved on methylamine as the sole carbon and energy source for 150 generations neither fitness nor growth rate improved. These results suggest that the NMG pathway permits slow growth on methylamine and is widely distributed in methylotrophs; however, rapid growth on methylamine can be achieved quite readily through acquisition of the mau cluster by HGT. View Full-Text
Keywords: Methylotrophy; Methylamine; Experimental Evolution; Methylobacterium; Horizontal Gene Transfer (HGT) Methylotrophy; Methylamine; Experimental Evolution; Methylobacterium; Horizontal Gene Transfer (HGT)
This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. (CC BY 4.0).

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MDPI and ACS Style

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 2015, 3, 60-79.

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