Bacterial virulence against an oceanic bloom-forming phytoplankter is mediated by algal DMSP

Abstract

Emiliania huxleyi is a bloom forming microalga that impacts the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide (DMS). Top-down regulation of E. huxleyi blooms is attributed to viruses and grazers, however, the possible involvement of algicidal bacteria in bloom demise is still elusive. We isolated from a North Atlantic E. huxleyi bloom a Roseobacter strain, Sulfitobacter D7, which exhibited algicidal effects against E. huxleyi upon coculturing. Both the alga and the bacterium were found to co-occur during a natural E. huxleyi bloom, therefore establishing this host-pathogen system as an attractive, ecologically relevant model for studying alga-bacterium interaction in the oceans. During interaction, Sulfitobacter D7 consumed and metabolized algal DMSP to produce high amounts of methanethiol, an alternative product of DMSP catabolism. We revealed a unique strain-specific response, in which E. huxleyi strains that exuded higher amounts of DMSP were more susceptible to Sulfitobacter D7 infection. Intriguingly, exogenous application of DMSP enhanced bacterial virulence and induced susceptibility in a resistant algal strain to the bacterial pathogen. This DMSP-dependent pathogenicity was highly specific as compared to supplementation of propionate and glycerol. We propose a novel function for DMSP, in addition to its central role in mutualistic interactions, as a mediator of bacterial virulence that may regulate E. huxleyi blooms. IntroductionPhytoplankton are unicellular, photosynthetic microorganisms that contribute to about half of the estimated global net primary production, and therefore serve as the basis of the marine food web (1,2). Biotic interactions can control the fate of phytoplankton blooms in the ocean, namely predation by zooplankton, viral infections and potentially algicidal activity of bacteria (3,4). One bacterial group highly associated with phytoplankton blooms is the Roseobacter clade (α-Proteobacteria) (5-8) which inhabits diverse marine environments and has a wide variety of metabolic capabilities (9-11).Moreover, Roseobacters were found to have a range of direct interactions, from cooperative to pathogenic, with phytoplankton species (12-16). These interactions are thought to be mediated by secreted infochemicals (17). Infochemical signaling occurs within the phycosphere, the micro-environment that surrounds algal cells where molecules can accumulate to relatively high effective concentrations (18)(19)(20)(21). The organosulfur compound dimethylsulfoniopropionate (DMSP), and its metabolic products, plays a key role in trophic-level interactions (17) and was suggested to act as an infochemical within the phycosphere (20,22). It is produced by diverse phytoplankton species (23) and is known to mediate algae-bacteria interaction by acting as a chemoattractant (24,25) and as sulfur and carbon sources for bacterial growth (14,26,27).Emiliania huxleyi is a cosmopolitan coccolithophore species which forms massiv...

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

“…huxleyi cells appears to mirror previous studies in which cellular arrest has been observed in phytoplankton in response to bacterially derived chemical exposure 19,20,21,22,23 , as well as nutrient limitation 24,25,26 . Indeed, at the physiological level, the response of E. huxleyi to HHQ parallels phosphorus (P) limitation in phytoplankton (i.e.…”

Complete Genome Sequence of Sulfitobacter sp. Strain D7, a Virulent Bacterium Isolated from an Emiliania huxleyi Algal Bloom in the North Atlantic

“…In total, there are 4 complete rRNA operons, 47 tRNAs, 3,744 protein-coding genes, and 52 pseudogenes, with all RNA genes located on the chromosome. Consistent with observation of the production of methanethiol, a metabolic by-product of DMSP, during coculturing with E. huxleyi , the chromosome encoded dmdA for demethylation of DMSP ( 2 ). In addition, we identified type I and type II secretion system genes on the chromosome and type IV genes on the plasmids p2SUD7 and p3SUD7, which may be involved in the bacterium’s interactions with the alga.…”

“…Here, we report the complete genome sequence of Sulfitobacter sp. strain D7, a Rhodobacterales bacterium that, when cocultured with E. huxleyi , causes death of the alga in a DMSP-dependent manner ( 2 ). It was isolated from the microbiome of copepods collected during a natural E. huxleyi bloom in the North Atlantic, and its cooccurrence with the alga in the water column was confirmed by quantitative PCR (qPCR) ( 2 ).…”

Ecological drivers of bacterial community assembly in synthetic phycospheres

“…S3) suggests ample opportunities for within-guild interactions in the form of competition or mutualisms (39)(40)(41). An additional level of microbial interactions occurs in natural phycospheres between bacteria and living phytoplankton that is not represented in this synthetic system; such interactions have been shown previously to encompass both mutualistic and antagonistic relationships (39,42,43).…”