Abstract
Shewanella spp. possess a broad respiratory versatility, which contributes to the occupation of hypoxic and anoxic environmental or host-associated niches. Here, we observe a strain-specific induction of biofilm formation in response to supplementation with the anaerobic electron acceptors dimethyl sulfoxide (DMSO) and nitrate in a panel of Shewanella algae isolates. The respiration-driven biofilm response is not observed in DMSO and nitrate reductase deletion mutants of the type strain S. algae CECT 5071, and can be restored upon complementation with the corresponding reductase operon(s) but not by an operon containing a catalytically inactive nitrate reductase. The distinct transcriptional changes, proportional to the effect of these compounds on biofilm formation, include cyclic di-GMP (c-di-GMP) turnover genes. In support, ectopic expression of the c-di-GMP phosphodiesterase YhjH of Salmonella Typhimurium but not its catalytically inactive variant decreased biofilm formation. The respiration-dependent biofilm response of S. algae may permit differential colonization of environmental or host niches.
Highlights
A hallmark of members of the genus Shewanella is their remarkable respiratory versatility since they can respire on an array of organic and inorganic compounds comprising virtually any electron acceptor more electronegative than sulfate[1,2]
While screening chemical libraries for biofilm inhibitors, we noticed that an addition of 35 mM dimethyl sulfoxide (DMSO) enhanced biofilm formation of S. algae CECT 5071 static cultures ~2-fold compared to the non-supplemented control
Since a similar phenomenon had not been observed with other DMSO-respiring bacteria, we reasoned that this phenotype could be specific to S. algae
Summary
A hallmark of members of the genus Shewanella is their remarkable respiratory versatility since they can respire on an array of organic and inorganic compounds comprising virtually any electron acceptor more electronegative than sulfate[1,2]. The respiratory capacity of Shewanella is reinforced by mediatordirected electron transfer mechanisms enabling the efficient reduction of insoluble substrates such as metal oxides[3]. This respiratory flexibility results in an extraordinary physiological versatility that contributes to the environmental abundance of the chemoorganotroph shewanellae as versatile colonizers of oxic, hypoxic, and anoxic marine and freshwater habitats[2]. Biofilm formation promotes the colonization of biotic and abiotic substrata in Shewanella spp. and many other bacterial species[6]. This predominantly sedentary lifestyle is a developmental process initiated by an attachment of single cells that subsequently form microcolonies prior to the establishment of mature biofilms. While biofilm formation on insoluble metal oxides has been well documented[19], knowledge on the behavioral and physiological biofilm responses upon use of the broad array of AEAs is limited in Shewanella species, as is the repertoire of terminal reductases enabling the respiration of AEAs
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