The results of empirical studies have revealed links between phytoplankton and bacterioplankton, such as the frequent correlation between chlorophyll a and bulk bacterial abundance and production. Nevertheless, little is known about possible links at the level of specific taxonomic groups. To investigate this issue, seawater microcosm experiments were performed in the northwestern Mediterranean Sea. Turbulence was used as a noninvasive means to induce phytoplankton blooms dominated by different algae. Microcosms exposed to turbulence became dominated by diatoms, while small phytoflagellates gained importance under still conditions. Denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments showed that changes in phytoplankton community composition were followed by shifts in bacterioplankton community composition, both as changes in the presence or absence of distinct bacterial phylotypes and as differences in the relative abundance of ubiquitous phylotypes. Sequencing of DGGE bands showed that four Roseobacter phylotypes were present in all microcosms. The microcosms with a higher proportion of phytoflagellates were characterized by four phylotypes of the Bacteroidetes phylum: two affiliated with the family Cryomorphaceae and two with the family Flavobacteriaceae. Two other Flavobacteriaceae phylotypes were characteristic of the diatom-dominated microcosms, together with one Alphaproteobacteria phylotype (Roseobacter) and one Gammaproteobacteria phylotype (Methylophaga). Phylogenetic analyses of published Bacteroidetes 16S rRNA gene sequences confirmed that members of the Flavobacteriaceae are remarkably responsive to phytoplankton blooms, indicating these bacteria could be particularly important in the processing of organic matter during such events. Our data suggest that quantitative and qualitative differences in phytoplankton species composition may lead to pronounced differences in bacterioplankton species composition.
Bacteroidetes are commonly assumed to be specialized in degrading high molecular weight (HMW) compounds and to have a preference for growth attached to particles, surfaces or algal cells. The first sequenced genomes of marine Bacteroidetes seemed to confirm this assumption. Many more genomes have been sequenced recently. Here, a comparative analysis of marine Bacteroidetes genomes revealed a life strategy different from those of other important phyla of marine bacterioplankton such as Cyanobacteria and Proteobacteria. Bacteroidetes have many adaptations to grow attached to particles, have the capacity to degrade polymers, including a large number of peptidases, glycoside hydrolases (GHs), glycosyl transferases, adhesion proteins, as well as the genes for gliding motility. Several of the polymer degradation genes are located in close association with genes for TonB-dependent receptors and transducers, suggesting an integrated regulation of adhesion and degradation of polymers. This confirmed the role of this abundant group of marine bacteria as degraders of particulate matter. Marine Bacteroidetes had a significantly larger number of proteases than GHs, while non-marine Bacteroidetes had equal numbers of both. Proteorhodopsin containing Bacteroidetes shared two characteristics: small genome size and a higher number of genes involved in CO 2 fixation per Mb. The latter may be important in order to survive when floating freely in the illuminated, but nutrient-poor, ocean surface.
Proteorhodopsins are bacterial light-dependent proton pumps. Their discovery within genomic material from uncultivated marine bacterioplankton caused considerable excitement because it indicated a potential phototrophic function within these organisms, which had previously been considered strictly chemotrophic. Subsequent studies established that sequences encoding proteorhodopsin are broadly distributed throughout the world's oceans. Nevertheless, the role of proteorhodopsins in native marine bacteria is still unknown. Here we show, from an analysis of the complete genomes of three marine Flavobacteria, that cultivated bacteria in the phylum Bacteroidetes, one of the principal components of marine bacterioplankton, contain proteorhodopsin. Moreover, growth experiments in both natural and artificial seawater (low in labile organic matter, which is typical of the world's oceans) establish that exposure to light results in a marked increase in the cell yield of one such bacterium (Dokdonia sp. strain MED134) when compared with cells grown in darkness. Thus, our results show that the phototrophy conferred by proteorhodopsin can provide critical amounts of energy, not only for respiration and maintenance but also for active growth of marine bacterioplankton in their natural environment.
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