The temperature-dependent expression of type II secretion system controls extracellular product secretion and virulence in mesophilic Aeromonas salmonida SRW-OG1

Abstract

Aeromonas salmonicida is a typical cold water bacterial pathogen that causes furunculosis in many freshwater and marine fish species worldwide. In our previous study, the pathogenic A. salmonicida (SRW-OG1) was isolated from a warm water fish, Epinephelus coioides was genomics and transcriptomics analyzed. Type II secretion system was found in the genome of A. salmonicida SRW-OG1, while the expressions of tatA, tatB, and tatC were significantly affected by temperature stress. Also, sequence alignment analysis, homology analysis and protein secondary structure function analysis showed that tatA, tatB, and tatC were highly conservative, indicating their biological significance. In this study, by constructing the mutants of tatA, tatB, and tatC, we investigated the mechanisms underlying temperature-dependent virulence regulation in mesophilic A. salmonida SRW-OG1. According to our results, tatA, tatB, and tatC mutants presented a distinct reduction in adhesion, hemolysis, biofilm formation and motility. Compared to wild-type strain, inhibition of the expression of tatA, tatB, and tatC resulted in a decrease in biofilm formation by about 23.66%, 19.63% and 40.13%, and a decrease in adhesion ability by approximately 77.69%, 80.41% and 62.14% compared with that of the wild-type strain. Furthermore, tatA, tatB, and tatC mutants also showed evidently reduced extracellular enzymatic activities, including amylase, protease, lipase, hemolysis and lecithinase. The genes affecting amylase, protease, lipase, hemolysis, and lecithinase of A. salmonicida SRW-OG1 were identified as cyoE, ahhh1, lipA, lipB, pulA, HED66_RS01350, HED66_RS19960, aspA, fabD, and gpsA, which were notably affected by temperature stress and mutant of tatA, tatB, and tatC. All above, tatA, tatB and tatC regulate the virulence of A. salmonicida SRW-OG1 by affecting biofilm formation, adhesion, and enzymatic activity of extracellular products, and are simultaneously engaged in temperature-dependent pathogenicity.

Comparative genomic analysis provides insights into taxonomy and temperature adaption of Aeromonas salmonicida

“…However, a wide infection caused by A. salmonicida has been reported in different species of fish worldwide, including rainbow trout ( Oncorhynchus mykiss ), Atlantic salmon ( Salmo salar ), arctic char ( Salvelinus alpinus ), brook trout ( Salvelinus fontinalis ), brown trout ( Salmo trutta ), carp ( Cyprinus carpio ), goldfish ( Carassius auratus ), orange‐spotted grouper ( Epinephelus coioiaes ) and sablefish ( Anoplopoma fimbria ) from Canada, USA, Switzerland, Norway, France, South Korea, Spain, Chile, China and so on (Bartkova et al, 2010; Charette et al, 2012; Evenberg et al, 1986; Huang, Qi, Zuo, Alias, & Xu, 2020; Humphrey & Ashburner, 1993; Pylkkö et al, 2005; Valderrama et al, 2019; Vasquez et al, 2020). In particular, it is worth noting that, more and more studies in China on infection (Lian et al, 2020; Meng et al, 2020; Wang et al, 2020), pathogenicity (Chen et al, 2022; Meng et al, 2017; Yi et al, 2022) and interaction with hosts of A. salmonicida (Huang, Qi, Zuo, Alias, & Xu, 2020; Long et al, 2015; Xia et al, 2022; Xue et al, 2021) have been reported in recent years, implying the popularity and importance of this bacterium in China.…”

“…. In particular, it is worth noting that, more and more studies in China on infection (Lian et al, 2020;Meng et al, 2020;Wang et al, 2020), pathogenicity (Chen et al, 2022;Meng et al, 2017;Yi et al, 2022) and interaction with hosts of A. salmonicida (Huang, Qi, Zuo, Alias, & Xu, 2020;Long et al, 2015;Xia et al, 2022;Xue et al, 2021) have been reported in recent years, implying the popularity and importance of this bacterium in China.…”

Temperature-specific adaptations and genetic requirements in a biofilm formed by Pseudomonas aeruginosa

“…The impact of temperature on the biofilm formation has been studied in several microbes including P. aeruginosa (Townsley and Yildiz, 2015;Townsley et al, 2016;Plumley et al, 2017;Kim et al, 2020;Almblad et al, 2021;del Peso Santos et al, 2021). Temperature is also known to cause stress in mesophilic pathogens found in cold water (Yi et al, 2022). Previous research has shown that temperature can indeed influence the gene expression and protein profile of P. aeruginosa at environmental versus host-associated temperatures (Bisht et al, 2021).…”