The Infection Process of Yersinia ruckeri: Reviewing the Pieces of the Jigsaw Puzzle

Abstract

Finding the keys to understanding the infectious process of Yersinia ruckeri was not a priority for many years due to the prompt development of an effective biotype 1 vaccine which was used mainly in Europe and USA. However, the gradual emergence of outbreaks in vaccinated fish, which have been reported since 2003, has awakened interest in the mechanism of virulence in this pathogen. Thus, during the last two decades, a large number of studies have considerably enriched our knowledge of many aspects of the pathogen and its interaction with the host. By means of both conventional and a variety of novel strategies, such as cell GFP tagging, bioluminescence imaging and optical projection tomography, it has been possible to determine three putative Y. ruckeri infection routes, the main point of entry for the bacterium being the gill lamellae. Moreover, a wide range of potential virulence factors have been highlighted by specific gene mutagenesis strategies or genome-wide transposon/plasmid insertion-based screening approaches, such us in vivo expression technology (IVET) and signature tagged mutagenesis (STM). Finally, recent proteomic and whole genomic analyses have allowed many of the genes and systems that are potentially implicated in the organism's pathogenicity and its adaptation to the host environmental conditions to be elucidated. Altogether, these studies contribute to a better understanding of the infectious process of Y. ruckeri in fish, which is crucial for the development of more effective strategies for preventing or treating enteric redmouth disease (ERM).

Keywords: Yersinia ruckeri; comparative genome; infection route; proteome analysis; virulence genes.

Figure 1

Bioluminescent tracking of Y. ruckeri harboring pCS26-Pac in a fish infected by bath immersion with 10⁷ cfu ml⁻¹ for 1 h. Bioluminescence emitted by the bacterium was captured three days postinfection by Ivis-Lumina equipment. Color standards represent “RLU max.” This measure expresses the highest number of counts in a pixel inside the region analyzed (Figure taken from Méndez and Guijarro, 2013).

Figure 2

Schematic representation of the Y. ruckeri systems related to virulence. See text for further details.

Figure 3

Cluster of genes absent from Y. ruckeri ATCC29473 type strain and present in the strains Y. ruckeri 150, CSF007-82, Big Creek and SC09. The region contains genes encoding for an enterobactin-like siderophore (blue), nine genes involved in the uptake and metabolism of citrate (yellow), a group of three genes related to hexose phosphate uptake (pink), three genes involved in iron transport (red) and a Crp-Fnr family transcriptional regulator (green). (1) Citrate succinate antiporter, (2) 2-(5′-triphosphoribosyl)-3′-dephosphocoenzyme-A synthase, (3) Apo-citrate lyase phosphoribosyldephospho-CoA transferase, (4) Citrate lyase alpha chain, (5) Citrate lyase beta chain, (6) Citrate lyase gamma chain acyl carrier protein, (7) [Citrate[pro-3S]-lyase] ligase, (8) Sensor kinase, (9) Transcriptional regulatory protein, (10) Transcriptional regulatory protein, (11) Sensor histidine protein kinase glucose-6-phosphate specific, (12) Hexose phosphate uptake regulatory protein, (13) Ferric iron ABC transporter iron-binding protein, (14) Ferric iron ABC transporter permease protein, (15) Ferric iron ABC transporter binding subunit (Figure taken from Cascales et al., 2017).