Analysis of genes encoding for proteolytic enzymes and cytotoxic proteins as virulence factors of <i>Piscirickettsia salmonis</i> in SHK‐1 cells

Figueroa, Jaime; Villagrán, Daniela; Cartes, C; Solís, Camila J.; Nourdin-Galindo, Guillermo; Haussmann, Denise

doi:10.1111/jfd.13333

Cited by 5 publications

(5 citation statements)

References 49 publications

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“…In addition, the downregulation of the ATP-dependent Clp protease involved in the proteolysis of defective and misfolded proteins (Aljghami et al, 2022) can be associated with the increased transcription of flagellin-related genes, similar to that described in mutants of S. typhimurium with a clpXP deletion (Tomoyasu et al, 2002). Moreover, it has been found to be modulated in P. salmonis during SHK-1 cell infection (Figueroa et al, 2021).…”

Section: Discussionsupporting

confidence: 52%

Cohabitation of Piscirickettsia salmonis genogroups (LF-89 and EM-90): synergistic effect on growth dynamics

Carril,

Winther-Larsen,

Løvoll

et al. 2023

Front. Cell. Infect. Microbiol.

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Piscirickettsia salmonis, the biological agent of Salmonid Rickettsial Septicemia (SRS), is a facultative intracellular bacterium that can be divided into two genogroups (LF-89 and EM-90) with different virulence levels and patterns. Studies have found co-infection of these genogroups in salmonid farms in Chile, but it is essential to assess whether this interaction within the host is related to virulence and changes in pathogen dynamics. In this study, we studied four isolates from EM-90 and one LF-89 isolate chosen based on their genomic differences. The aim was to evaluate how co-cultivation affects bacterial growth performance and virulence factor expression in Atlantic salmon (Salmo salar) in vitro and in vivo. In vitro results using FN2 medium, showed a similar growth curve between co-cultures of LF-89 and EM-90 compared to EM-90 monocultures. This was explained by the higher ratio of EM-90 to LF-89 in all co-cultures. When evaluating the expression of virulence factors, it was discovered that the luxR gene was expressed only in EM-90-like isolates and that there were significant differences between mono- and co-cultures for flaA and cheA, suggesting a response to cohabitation. Moreover, during in vivo co-cultures, transcriptomic analysis revealed an upregulation of transposases, flagellum-related genes (fliI and flgK), transporters, and permeases that could unveil novel virulence effectors used in the early infection process of P. salmonis. Thus, our work has shown that cohabitation of P. salmonis genogroups can modulate their behavior and virulence effector expression. These data can contribute to new strategies and approaches to improve the current health treatments against this salmonid pathogen.

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Section: Discussionsupporting

confidence: 52%

Cohabitation of Piscirickettsia salmonis genogroups (LF-89 and EM-90): synergistic effect on growth dynamics

Carril,

Winther-Larsen,

Løvoll

et al. 2023

Front. Cell. Infect. Microbiol.

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“…Aligning with this finding, clpP gene expression can increase once P . salmonis LF-89 T infects the SHK-1 cell line ( Figueroa et al., 2021 ). In addition, an alkyl hydroperoxide reductase (AhpC), involved in potential protection against oxidative stress ( Oh and Jeon, 2014 ), was encoded by a DEG upregulated in 24-h-old biofilms and downregulated in 48-h-old biofilms (Gene 938 in Supplementary Tables S6, S9 ).…”

Section: Discussionmentioning

confidence: 99%

“…salmonis actives virulence genes (e.g., dot / icm homologue genes, protease-encoding genes, etc.) ( Gómez et al., 2013 ; Labra et al., 2016 ; Figueroa et al., 2021 ) and generates several proteins ( Ortiz-Severín et al., 2020 ) with virulence properties; these features can co-occur with a generalized translational arrest ( Zúñiga et al., 2020 ). Some of these activated genes (e.g., clpB , bipA , dot / icm ) participate in intracellular survival ( Isla et al., 2014 ; Machuca and Martinez, 2016 ) or biofilm-formation regulation (e.g., stringent response genes) ( Díaz-Salazar et al., 2017 ; Zúñiga et al., 2020 ), with intracellular infection state-dependent levels of gene expression ( Ortiz-Severín et al., 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Collective behavior and virulence arsenal of the fish pathogen Piscirickettsia salmonis in the biofilm realm

Levipan

Irgang

Opazo

et al. 2022

Front. Cell. Infect. Microbiol.

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Piscirickettsiosis is a fish disease caused by the Gram-negative bacterium Piscirickettsia salmonis. This disease has a high socio-economic impact on the Chilean salmonid aquaculture industry. The bacterium has a cryptic character in the environment and their main reservoirs are yet unknown. Bacterial biofilms represent a ubiquitous mechanism of cell persistence in diverse natural environments and a risk factor for the pathogenesis of several infectious diseases, but their microbiological significance for waterborne veterinary diseases, including piscirickettsiosis, have seldom been evaluated. This study analyzed the in vitro biofilm behavior of P. salmonis LF-89T (genogroup LF-89) and CA5 (genogroup EM-90) using a multi-method approach and elucidated the potential arsenal of virulence of the P. salmonis LF-89T type strain in its biofilm state. P. salmonis exhibited a quick kinetics of biofilm formation that followed a multi-step and highly strain-dependent process. There were no major differences in enzymatic profiles or significant differences in cytotoxicity (as tested on the Chinook salmon embryo cell line) between biofilm-derived bacteria and planktonic equivalents. The potential arsenal of virulence of P. salmonis LF-89T in biofilms, as determined by whole-transcriptome sequencing and differential gene expression analysis, consisted of genes involved in cell adhesion, polysaccharide biosynthesis, transcriptional regulation, and gene mobility, among others. Importantly, the global gene expression profiles of P. salmonis LF-89T were not enriched with virulence-related genes upregulated in biofilm development stages at 24 and 48 h. An enrichment in virulence-related genes exclusively expressed in biofilms was also undetected. These results indicate that early and mature biofilm development stages of P. salmonis LF-89T were transcriptionally no more virulent than their planktonic counterparts, which was supported by cytotoxic trials, which, in turn, revealed that both modes of growth induced important and very similar levels of cytotoxicity on the salmon cell line. Our results suggest that the aforementioned biofilm development stages do not represent hot spots of virulence compared with planktonic counterparts. This study provides the first transcriptomic catalogue to select specific genes that could be useful to prevent or control the (in vitro and/or in vivo) adherence and/or biofilm formation by P. salmonis and gain further insights into piscirickettsiosis pathogenesis.

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“…P. salmonis can synthesize and secrete siderophores ( 81 ), confirming its ability to utilize different sources of iron. In addition, P. salmonis has protease activity that increases significantly when the bacterium infects cells ( 62 ). At the same time, genomic islands have been described in the genomes of different P. salmonis strains ( 73 ), which could explain the different virulence levels of P. salmonis genogroups, pathogenesis ( 8 , 14 ) and immune response observed in both fish experimentally challenged with different P. salmonis genogroups and vaccinated fish ( 11 , 12 , 14 , 29 ).…”

Section: Piscirickettsia Salmonis : a Fastidious Bacteriummentioning

confidence: 99%

Why Does Piscirickettsia salmonis Break the Immunological Paradigm in Farmed Salmon? Biological Context to Understand the Relative Control of Piscirickettsiosis

Rozas‐Serri¹

2022

Front. Immunol.

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Piscirickettsiosis (SRS) has been the most important infectious disease in Chilean salmon farming since the 1980s. It was one of the first to be described, and to date, it continues to be the main infectious cause of mortality. How can we better understand the epidemiological situation of SRS? The catch-all answer is that the Chilean salmon farming industry must fight year after year against a multifactorial disease, and apparently only the environment in Chile seems to favor the presence and persistence of Piscirickettsia salmonis. This is a fastidious, facultative intracellular bacterium that replicates in the host’s own immune cells and antigen-presenting cells and evades the adaptive cell-mediated immune response, which is why the existing vaccines are not effective in controlling it. Therefore, the Chilean salmon farming industry uses a lot of antibiotics—to control SRS—because otherwise, fish health and welfare would be significantly impaired, and a significantly higher volume of biomass would be lost per year. How can the ever-present risk of negative consequences of antibiotic use in salmon farming be balanced with the productive and economic viability of an animal production industry, as well as with the care of the aquatic environment and public health and with the sustainability of the industry? The answer that is easy, but no less true, is that we must know the enemy and how it interacts with its host. Much knowledge has been generated using this line of inquiry, however it remains insufficient. Considering the state-of-the-art summarized in this review, it can be stated that, from the point of view of fish immunology and vaccinology, we are quite far from reaching an effective and long-term solution for the control of SRS. For this reason, the aim of this critical review is to comprehensively discuss the current knowledge on the interaction between the bacteria and the host to promote the generation of more and better measures for the prevention and control of SRS.

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Analysis of genes encoding for proteolytic enzymes and cytotoxic proteins as virulence factors of Piscirickettsia salmonis in SHK‐1 cells

Cited by 5 publications

References 49 publications

Cohabitation of Piscirickettsia salmonis genogroups (LF-89 and EM-90): synergistic effect on growth dynamics

Cohabitation of Piscirickettsia salmonis genogroups (LF-89 and EM-90): synergistic effect on growth dynamics

Collective behavior and virulence arsenal of the fish pathogen Piscirickettsia salmonis in the biofilm realm

Why Does Piscirickettsia salmonis Break the Immunological Paradigm in Farmed Salmon? Biological Context to Understand the Relative Control of Piscirickettsiosis

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