Comparative genomics of cyclic di-GMP metabolism and chemosensory pathways in Shewanella algae strains: novel bacterial sensory domains and functional insights into lifestyle regulation

Shewanella spp. play important ecological and biogeochemical roles, due in part to their versatile metabolism and swift integration of stimuli. While Shewanella spp. are primarily considered environmental microbes, Shewanella algae is increasingly recognized as an occasional human pathogen. S. algae shares the broad metabolic and respiratory repertoire of Shewanella spp. and thrives in similar ecological niches. In S. algae, nitrate and dimethyl sulfoxide (DMSO) respiration promote biofilm formation strain specifically, with potential implication of taxis and cyclic diguanosine monophosphate (c-di-GMP) signaling. Signal transduction systems in S. algae have not been investigated. To fill these knowledge gaps, we provide here an inventory of the c-di-GMP turnover proteome and chemosensory networks of the type strain S. algae CECT 5071 and compare them with those of 41 whole-genome-sequenced clinical and environmental S. algae isolates. Besides comparative analysis of genetic content and identification of laterally transferred genes, the occurrence and topology of c-di-GMP turnover proteins and chemoreceptors were analyzed. We found S. algae strains to encode 61 to 67 c-di-GMP turnover proteins and 28 to 31 chemoreceptors, placing S. algae near the top in terms of these signaling capacities per Mbp of genome. Most c-di-GMP turnover proteins were predicted to be catalytically active; we describe in them six novel N-terminal sensory domains that appear to control their catalytic activity. Overall, our work defines the c-di-GMP and chemosensory signal transduction pathways in S. algae, contributing to a better understanding of its ecophysiology and establishing S. algae as an auspicious model for the analysis of metabolic and signaling pathways within the genus Shewanella.
Funding for this study was provided by grants from Stiftelsen Lars Hiertas Minne (grant FO2019‐0293), Stiftelsen Längmanska Kulturfonden (grant BA20‐0736), the Karolinska Institute Research Foundation (grant 2020‐01556), Stiftelsen Anna och Gunnar Vidfelts fond för biologisk forskning (grant 2019-051-Vidfelts fond/SOJOH) and the Hans Dahlbergs Stiftelse för miljö och hälsa to A.J.M.-R. M.Y.G. was supported by the Intramural Research Program of the National Library of Medicine, U.S. National Institutes of Health. T.K. was supported by grants from the Junta de Andalucía (P18-FR-1621) and the Spanish Ministry of Economy and Competitiveness (PID2020-112612GB-I00). U.R. was supported by the Swedish Research Council for Natural Sciences and Engineering (2017-04465) and the Karolinska Institute.