High abundance of virulence gene homologues in marine bacteria

Abstract

Marine bacteria can cause harm to single-celled and multicellular eukaryotes. However, relatively little is known about the underlying genetic basis for marine bacterial interactions with higher organisms. We examined whole-genome sequences from a large number of marine bacteria for the prevalence of homologues to virulence genes and pathogenicity islands known from bacteria that are pathogenic to terrestrial animals and plants. As many as 60 out of 119 genomes of marine bacteria, with no known association to infectious disease, harboured genes of virulence-associated types III, IV, V and VI protein secretion systems. Type III secretion was relatively uncommon, while type IV was widespread among alphaproteobacteria (particularly among roseobacters) and type VI was primarily found among gammaproteobacteria. Other examples included homologues of the Yersinia murine toxin and a phage-related 'antifeeding' island. Analysis of the Global Ocean Sampling metagenomic data indicated that virulence genes were present in up to 8% of the planktonic bacteria, with highest values in productive waters. From a marine ecology perspective, expression of these widely distributed genes would indicate that some bacteria infect or even consume live cells, that is, generate a previously unrecognized flow of organic matter and nutrients directly from eukaryotes to bacteria.

Fig. 1

Gene organization of T6SSs in five representatives of the marine bacteria compared with those of Salmonella enterica subsp. I, Rhizobium leguminosarum biovar trifolii, and Vibrio cholerae O1 biovar eltor str. N16961. Predicted gene homologues are depicted with the same colours and patterns. The following genetic regions are shown: Photobacterium sp. SKA34 (SKA34_05615 to SKA34_05715), Oceanobacter sp. RED65 (RED65_00815 to RED65_00895), Reinekea sp. MED297 (MED297_18458 to MED297_18883), Vibrio sp. MED222 (MED222_13880 to MED222_13980), Marinomonas sp. MED121 (#1: genes MED121_07350 to MED121_07465; #2: MED121_11870 to MED121_11955), Roseobacter sp. MED193 (MED193_00960 to MED193_01055).

Fig. 2

Gene organization of the ‘antifeeding’ prophage-like island in marine bacteria. Genes that are predicted homologues to S. entomophila‘antifeeding’ genes are shown with the same patterns as these. Unfilled boxes indicate genes that do not have homologues in S. entomophila. Filled black circles above genes indicate genes that show similarity to phage structural genes. Black circles above genes of S. entomophila indicate genes that have been shown to be essential for the antifeeding effect of S. entomophila. S. entom: Serratia entomophila A1MO2 AND4, Vibrio campbellii AND4; MED217, Leeuwenhoekiella blandensis MED217; HTCC2594, Erythrobacter litoralis HTCC2594; NB231, Nitrococcus mobilis Nb-231 (two loci); NB311A, Nitrobacter sp. Nb311A; HTCC2654, Rhodobacterales bacterium HTCC2654.