Present address: Biology Department, Woods Hole Oceanographic Institution, Wods Hole, MA, USA.
Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides
Article first published online: 19 APR 2012
© 2012 Society for Applied Microbiology and Blackwell Publishing Ltd
Special Issue: Microbial Communities - Structure, Behaviour, Evolution
Volume 14, Issue 9, pages 2379–2394, September 2012
How to Cite
Thomas, F., Barbeyron, T., Tonon, T., Génicot, S., Czjzek, M. and Michel, G. (2012), Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environmental Microbiology, 14: 2379–2394. doi: 10.1111/j.1462-2920.2012.02751.x
- Issue published online: 4 SEP 2012
- Article first published online: 19 APR 2012
- Received 15 July, 2011; revised 19 March, 2012; accepted 21 March, 2012.
Alginate constitutes a significant part of seaweed biomass and thus a crucial nutrient for numerous marine heterotrophic bacteria. However, the mechanisms for alginate assimilation remain largely unknown in marine microorganisms. We show here that the genome of the marine flavobacterium Zobellia galactanivorans contains seven putative alginate lyase genes, five of them localized within two clusters comprising additional carbohydrate-related genes. The transcription of these genes and the alginolytic activity were strongly induced when Z. galactanivorans used alginate as sole carbon source. These clusters were shown to be transcribed as polycistronic mRNAs and thus to constitute operons. Several candidate enzymes were successfully overexpressed in Escherichia coli, purified and their activity tested. Particularly, AlyA1, AlyA4, AlyA5 and AlyA7 are confirmed as active alginate lyases. Zg2622 and Zg2614 are a dehydrogenase and a kinase, respectively, further converting the terminal unsaturated monosaccharides released by alginate lyases into 2-keto-3-deoxy-6-phosphogluconate. In-depth phylogenomic analyses reveal that such alginolytic operons originated from an ancestral marine flavobacterium and were independently transferred to marine proteobacteria and Japanese gut Bacteroides. These bacteria thus gained the capacity to assimilate the main polysaccharide of brown algae, an adaptive advantage in coastal environments but also in the gut microbiota of specific human population.