Coordinated transcriptional response to environmental stress by a Synechococcus virus.

Viruses are a major control on populations of microbes. Often, their virulence is examined in controlled laboratory conditions. Yet, in nature, environmental conditions lead to changes in host physiology and fitness that may impart both costs and benefits on viral success. Phosphorus (P) is a major abiotic control on the marine cyanobacterium Synechococcus. Some viruses infecting Synechococcus have acquired, from their host, a gene encoding a P substrate binding protein (PstS), thought to improve virus replication under phosphate starvation. Yet, pstS is uncommon among cyanobacterial viruses. Thus, we asked how infections with viruses lacking PstS are affected by P scarcity. We show that the production of infectious virus particles of such viruses is reduced in low P conditions. However, this reduction in progeny is not caused by impaired phage genome replication, thought to be a major sink for cellular phosphate. Instead, transcriptomic analysis showed that under low P conditions, a PstS-lacking cyanophage increased the expression of a specific gene set that included mazG, hli2, and gp43 encoding a pyrophosphatase, a high-light inducible protein and DNA polymerase, respectively. Moreover, several of the upregulated genes were controlled by the host's phoBR two-component system. We hypothesize that recycling and polymerization of nucleotides liberates free phosphate and thus allows viral morphogenesis, albeit at lower rates than when phosphate is replete or when phages encode pstS. Altogether, our data show how phage genomes, lacking obvious P-stress-related genes, have evolved to exploit their host's environmental sensing mechanisms to coordinate their own gene expression in response to resource limitation.

Elucidation of glutamine lipid biosynthesis in marine bacteria reveals its importance under phosphorus deplete growth in Rhodobacteraceae.

Marine microorganisms employ multiple strategies to cope with transient and persistent nutrient limitation, one of which, for alleviating phosphorus (P) stress, is to substitute membrane glycerophospholipids with non-P containing surrogate lipids. Such a membrane lipid remodelling strategy enables the most abundant marine phytoplankton and heterotrophic bacteria to adapt successfully to nutrient scarcity in marine surface waters. An important group of non-P lipids, the aminolipids which lack a diacylglycerol backbone, are poorly studied in marine microbes. Here, using a combination of genetic, lipidomics and metagenomics approaches, we reveal for the first time the genes (glsB, olsA) required for the formation of the glutamine-containing aminolipid. Construction of a knockout mutant in either glsB or olsA in the model marine bacterium Ruegeria pomeroyi DSS-3 completely abolished glutamine lipid production. Moreover, both mutants showed a considerable growth cost under P-deplete conditions and the olsA mutant, that is unable to produce the glutamine and ornithine aminolipids, ceased to grow under P-deplete conditions. Analysis of sequenced microbial genomes show that glsB is primarily confined to the Rhodobacteraceae family, which includes the ecologically important marine Roseobacter clade that are key players in the marine sulphur and nitrogen cycles. Analysis of the genes involved in glutamine lipid biosynthesis in the Tara ocean metagenome dataset revealed the global occurrence of glsB in marine surface waters and a positive correlation between glsB abundance and N* (a measure of the deviation from the canonical Redfield ratio), suggesting glutamine lipid plays an important role in the adaptation of marine Rhodobacteraceae to P limitation.