Screening of metagenomic and genomic libraries reveals three classes of bacterial enzymes that overcome the toxicity of acrylate

Curson, Andrew R. J., Burns, Oliver J., Voget, Sonja, Daniel, Rolf, Todd, Jonathan D., McInnis, Kathryn, Wexler, Margaret and Johnston, Andrew W. B. (2014) Screening of metagenomic and genomic libraries reveals three classes of bacterial enzymes that overcome the toxicity of acrylate. PLoS One, 9 (5). ISSN 1932-6203

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Abstract

Acrylate is produced in significant quantities through the microbial cleavage of the highly abundant marine osmoprotectant dimethylsulfoniopropionate, an important process in the marine sulfur cycle. Acrylate can inhibit bacterial growth, likely through its conversion to the highly toxic molecule acrylyl-CoA. Previous work identified an acrylyl-CoA reductase, encoded by the gene acuI, as being important for conferring on bacteria the ability to grow in the presence of acrylate. However, some bacteria lack acuI, and, conversely, many bacteria that may not encounter acrylate in their regular environments do contain this gene. We therefore sought to identify new genes that might confer tolerance to acrylate. To do this, we used functional screening of metagenomic and genomic libraries to identify novel genes that corrected an E. coli mutant that was defective in acuI, and was therefore hyper-sensitive to acrylate. The metagenomic libraries yielded two types of genes that overcame this toxicity. The majority encoded enzymes resembling AcuI, but with significant sequence divergence among each other and previously ratified AcuI enzymes. One other metagenomic gene, arkA, had very close relatives in Bacillus and related bacteria, and is predicted to encode an enoyl-acyl carrier protein reductase, in the same family as FabK, which catalyses the final step in fatty-acid biosynthesis in some pathogenic Firmicute bacteria. A genomic library of Novosphingobium, a metabolically versatile alphaproteobacterium that lacks both acuI and arkA, yielded vutD and vutE, two genes that, together, conferred acrylate resistance. These encode sequential steps in the oxidative catabolism of valine in a pathway in which, significantly, methacrylyl-CoA is a toxic intermediate. These findings expand the range of bacteria for which the acuI gene encodes a functional acrylyl-CoA reductase, and also identify novel enzymes that can similarly function in conferring acrylate resistance, likely, again, through the removal of the toxic product acrylyl-CoA.

Item Type:	Article
Additional Information:	© 2014 Curson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Uncontrolled Keywords:	sdg 14 - life below water ,/dk/atira/pure/sustainabledevelopmentgoals/life_below_water
Faculty \ School:	Faculty of Science > School of Biological Sciences Faculty of Science
UEA Research Groups:	Faculty of Science > Research Groups > Environmental Biology Faculty of Science > Research Groups > Resources, Sustainability and Governance (former - to 2018) Faculty of Science > Research Groups > Molecular Microbiology
Depositing User:	Pure Connector
Date Deposited:	19 Aug 2014 14:30
Last Modified:	25 Sep 2024 11:26
URI:	https://ueaeprints.uea.ac.uk/id/eprint/49943
DOI:	10.1371/journal.pone.0097660

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