Vibrio fischeri imports and assimilates sulfate during symbiosis with Euprymna scolopes

• Published in: Molecular microbiology 2021-09, Vol.116 (3), p.926-942
• Main Authors: Wasilko, Nathan P., Ceron, Josue S., Baker, Emily R., Cecere, Andrew G., Wollenberg, Michael S., Miyashiro, Tim I.
• Format: Article
• Language: English
• Subjects: Aliivibrio fischeri - physiology; Animals; Assimilation; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biological Transport; Bioluminescence; Cysteine; Cysteine - metabolism; Decapodiformes - microbiology; Genes; Genomes; Host Microbial Interactions; host–microbe interactions; Imports; In vivo methods and tests; Marine environment; Membrane Transport Proteins - genetics; Membrane Transport Proteins - metabolism; Molecular modelling; Mutagenesis; Mutants; Mutation; Phenotypes; Phylogeny; Squid; sulfate assimilation; Sulfates; Sulfates - metabolism; Sulfur; Sulfur - metabolism; Symbiosis; transport; Transposon mutagenesis; Vibrio; Vibrio fischeri
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.14780

Sulfur is in cellular components of bacteria and is, therefore, an element necessary for growth. However, mechanisms by which bacteria satisfy their sulfur needs within a host are poorly understood. Vibrio fischeri is a bacterial symbiont that colonizes, grows, and produces bioluminescence within the light organ of the Hawaiian bobtail squid, which provides an experimental platform for investigating sulfur acquisition in vivo. Like other γ‐proteobacteria, V. fischeri fuels sulfur‐dependent anabolic processes with intracellular cysteine. Within the light organ, the abundance of a ΔcysK mutant, which cannot synthesize cysteine through sulfate assimilation, is attenuated, suggesting sulfate import is necessary for V. fischeri to establish symbiosis. Genes encoding sulfate‐import systems of other bacteria that assimilate sulfate were not identified in the V. fischeri genome. A transposon mutagenesis screen implicated YfbS as a sulfate importer. YfbS is necessary for growth on sulfate and in the marine environment. During symbiosis, a ΔyfbS mutant is attenuated and strongly expresses sulfate‐assimilation genes, which is a phenotype associated with sulfur‐starved cells. Together, these results suggest V. fischeri imports sulfate via YfbS within the squid light organ, which provides insight into the molecular mechanisms by which bacteria harvest sulfur in vivo. The bacterium Vibrio fischeri must acquire sulfur while establishing symbiosis within the squid light organ. In addition to a host‐derived sulfur source related to cystine, V. fischeri assimilates sulfate in vivo. We provide evidence that sulfate import is mediated by the transporter YfbS, which is widely distributed among other Vibrionaceae members.