Temperature-dependent expression of virulence genes in fish-pathogenic bacteria

Abstract

Virulence gene expression in pathogenic bacteria is modulated by environmental parameters. A key factor in this expression is temperature. Its effect on virulence gene expression in bacteria infecting warm-blooded hosts is well documented. Transcription of virulence genes in these bacteria is induced upon a shift from low environmental to a higher host temperature (37°C). Interestingly, host temperatures usually correspond to the optimum for growth of these pathogenic bacteria. On the contrary, in ectothermic hosts such as fish, molluscs, and amphibians, infection processes generally occur at a temperature lower than that for the optimal growth of the bacteria. Therefore, regulation of virulence gene expression in response to temperature shift has to be modulated in a different way to that which is found in bacteria infecting warm-blooded hosts. The current understanding of virulence gene expression and its regulation in response to temperature in fish-pathogenic bacteria is limited, but constant extension of our knowledge base is essential to enable a rational approach to the problem of the bacterial fish diseases affecting the aquaculture industry. This is an interesting issue and progress needs to be made in order to diminish the economic losses caused by these diseases. The intention of this review is, for the first time, to compile the scattered results existing in the field in order to lay the groundwork for future research. This article is an overview of those relevant virulence genes that are expressed at temperatures lower than that for optimal bacterial growth in different fish-pathogenic bacteria as well as the principal mechanisms that could be involved in their regulation.

Transcriptomic Analysis of Laribacter hongkongensis Reveals Adaptive Response Coupled with Temperature

“…hongkongensis obtained iron through multiple pathways to maintain iron homeostasis which in turn, play roles in the pathogenesis of fish infection at freshwater temperature. Noteworthy, iron sequestering systems were often found to be temperature-regulated and overexpressed at temperatures below that of their optimal growth (TBO) in other fish pathogens, which are similar to other virulence factors such as bacteriolysis-related proteins and secretion systems [55]. …”

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

“…In theory, virulence will evolve to a level at which virulence and transmission are balanced to optimize the spread of the pathogen (Alizon, Hurford, Mideo, & Van Baalen, 2009). Nevertheless, virulence is context–dependent, as both biotic factors such as host condition (Pulkkinen & Ebert, 2004) and host density (Bieger & Ebert, 2009) and abiotic factors such as temperature (Guijarro, Cascales, García‐Torrico, García‐Domínguez, & Méndez, 2015) can influence virulence. Consequently, pathogens that are able to survive outside their hosts and therefore less dependent on direct contact transmission are likely to experience nonoptimal virulence, high or low, depending on various factors that affects virulence outside the host (Bull & Ebert, 2008; Sundberg et al., 2014; Walther & Ewald, 2004).…”

“…Therefore, there will be an opportunity for increasing virulence and more potential for deadly outbreaks in future Finnish aquaculture due to the following reason(s): (a) Ambient temperatures in the Finnish farming environment rarely exceed 25°C, (b) Guijarro et al. (2015) showed that some bacterial diseases in aquaculture, particularly those of freshwater fish, could occur at temperatures below bacterial optimal growth (i.e., optimum growth temperature for the fastest growth under laboratory conditions), (c) the summer water temperature in the fish farms could potentially be kept under relative control in some flow‐through farm systems due to the mixing of ground water with the inflow water from natural bodies. Yet, F. columnare occurs globally and negative association of virulence with CT 50/high provides relevant information for tropical environments where water temperature may exceed 30°C.…”

“…For environmentally growing opportunist pathogens, adaptations for more efficient exploitation of one growth environment could be expected to cause repercussions in their ability to grow in the other environment (Brown et al., 2012), such as host environment. Alternatively, the presence of virulence factors in the bacteria is unnecessary during the planktonic state but essential for the infection process, helping bacteria to save energy by not expressing virulence genes until they sense they have entered the host environment (Guijarro et al., 2015). This could explain why more generalist strains with broader thermal performance breadth were less virulent than strains with narrower TPB (see: PC1 effect in Table 3 and Figure 4a).…”

High Nutrient Concentration Can Induce Virulence Factor Expression and Cause Higher Virulence in an Environmentally Transmitted Pathogen

“…As the environment outside the host is unpredictable, the bacteria have to adapt rapidly to the surrounding conditions, e.g. temperature [16] or nutrients [21]. Furthermore, environmentally transmitted pathogens need to have capacity for the invasion when a potential host is encountered, but the production of virulence factors in the absence of a host is costly.…”