The Expression of Virulence Factors in Vibrio anguillarum Is Dually Regulated by Iron Levels and Temperature

Abstract

Vibrio anguillarum causes a hemorrhagic septicemia that affects cold- and warm-water adapted fish species. The main goal of this work was to determine the temperature-dependent changes in the virulence factors that could explain the virulence properties of V. anguillarum for fish cultivated at different temperatures. We have found that although the optimal growth temperature is around 25°C, the degree of virulence of V. anguillarum RV22 is higher at 15°C. To explain this result, an RNA-Seq analysis was performed to compare the whole transcriptome profile of V. anguillarum RV22 cultured under low-iron availability at either 25 or 15°C, which would mimic the conditions that V. anguillarum finds during colonization of fish cultivated at warm- or cold-water temperatures. The comparative analysis of transcriptomes at high- and low-iron conditions showed profound metabolic adaptations to grow under low iron. These changes were characterized by a down-regulation of the energetic metabolism and the induction of virulence-related factors like biosynthesis of LPS, production of hemolysins and lysozyme, membrane transport, heme uptake, or production of siderophores. However, the expression pattern of virulence factors under iron limitation showed interesting differences at warm and cold temperatures. Chemotaxis, motility, as well as the T6SS1 genes are expressed at higher levels at 25°C than at 15°C. By contrast, hemolysin RTX pore-forming toxin, T6SS2, and the genes associated with exopolysaccharides synthesis were preferentially expressed at 15°C. Notably, at this temperature, the siderophore piscibactin system was strongly up-regulated. In contrast, at 25°C, piscibactin genes were down-regulated and the vanchrobactin siderophore system seems to supply all the necessary iron to the cell. The results showed that V. anguillarum adjusts the expression of virulence factors responding to two environmental signals, iron levels and temperature. Thus, the relative relevance of each virulence factor for each fish species could vary depending on the water temperature. The results give clues about the physiological adaptations that allow V. anguillarum to cause infections in different fishes and could be relevant for vaccine development against fish vibriosis.

The Effect of the Environmental Temperature on the Adaptation to Host in the Zoonotic Pathogen Vibrio vulnificus

“…In fact, V. vulnificus is able to cause severe septicemia at both 28 • C (in warm fish species) and 37 • C (in humans). Although temperaturedependent gene expression has been widely studied in other bacterial species (Gao et al, 2006;Wang et al, 2017;Matanza and Osorio, 2018;Lages et al, 2019), to our knowledge this is the first time that the global transcriptomic response to an increase in the environmental temperature is analyzed in V. vulnificus. Nevertheless, it is well known that temperature impacts V. vulnificus growth ability (Kim Y. W. et al, 2012) and the expression of some virulence factors such as the major protease (Vvp), iron uptake systems (HupA and VuuA) and quorum sensing (McDougald et al, 2001;Oh et al, 2009;Kim et al, 2016;Elgaml and Miyoshi, 2017).…”

Prevalence, virulence genes, and antimicrobial resistance of Vibrio species isolated from diseased marine fish in South China

“…High-density farming, along with intense human activities and global climate change, has led to frequent vibriosis, antibiotic overuse, and antibiotic resistance in recent years 6,29 . To thoroughly deploy the "Green and Healthy Aquaculture" initiative launched in 2020, the Ministry of Agriculture and Rural Affairs decided to implement "Drug Reduction in Aquaculture" and "Ecological Health Breeding" initiatives for the development of aquaculture animal disease detection, pathogen resistance monitoring, determination of suitable local antimicrobial profiles for aquaculture, provision of guidance for scientific medication, and promotion of vaccine use for disease prevention.…”

A Hopeful Sea-Monster: A Very Large Homologous Recombination Event Impacting the Core Genome of the Marine Pathogen Vibrio anguillarum

“…In addition to the large recombination event, we also examined diversity within two LPS and capsule synthesis gene clusters previously identified by Castillo et al (2017), which are positioned approximately 70-kb from the large recombination block. LPS is known to play an important role in immune evasion and adherence in V. anguillarum (Lindell et al, 2012), and the expression of genes coding for LPS production, transport and assembly is linked to environmental stresses such as low temperature and low iron availability (Lages et al, 2019). Here, we also note associations between gene content and nucleotide variation in these elements with serotype definition.…”