Biofilm is associated with chronic streptococcal meningoencephalitis in fish

Isiaku, Abdulsalam I.; Sabri, M. Y.; Yasin, Ina Salwany Md; Hassan, Muhammad Rosdi Abu; Tanko, Polycarp Nwunuji; Bello, Muhammad Bashir

doi:10.1016/j.micpath.2016.10.029

Cited by 20 publications

(12 citation statements)

References 52 publications

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“…It is currently unknown if P. salmonis biofilms or dispersed bacteria from these structures (as single-cell entities and/or aggregates) are involved in acute and/or chronic forms of the disease. However, considering the capacity of P. salmonis to form microcolony-like aggregations in tissues (e.g., in the skeletal muscle of rainbow trout 42 ), the participation of biofilm-related structures (e.g., the piscirickettsial attachment complex 13 ) during piscirickettsiosis cannot be ruled out, especially in chronic cases, such as with bacterial biofilms involved in other fish pathologies 54 .…”

Section: Discussionmentioning

confidence: 99%

Improved understanding of biofilm development by Piscirickettsia salmonis reveals potential risks for the persistence and dissemination of piscirickettsiosis

Levipan

Irgang

Yáñez

et al. 2020

Sci Rep

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Piscirickettsia salmonis is the causative agent of piscirickettsiosis, a disease with high socioeconomic impacts for Chilean salmonid aquaculture. The identification of major environmental reservoirs for P. salmonis has long been ignored. Most microbial life occurs in biofilms, with possible implications in disease outbreaks as pathogen seed banks. Herein, we report on an in vitro analysis of biofilm formation by P. salmonis Psal-103 (LF-89-like genotype) and Psal-104 (EM-90-like genotype), the aim of which was to gain new insights into the ecological role of biofilms using multiple approaches. The cytotoxic response of the salmon head kidney cell line to P. salmonis showed interisolate differences, depending on the source of the bacterial inoculum (biofilm or planktonic). Biofilm formation showed a variable-length lag-phase, which was associated with wider fluctuations in biofilm viability. Interisolate differences in the lag phase emerged regardless of the nutritional content of the medium, but both isolates formed mature biofilms from 288 h onwards. Psal-103 biofilms were sensitive to Atlantic salmon skin mucus during early formation, whereas Psal-104 biofilms were more tolerant. The ability of P. salmonis to form viable and mucus-tolerant biofilms on plastic surfaces in seawater represents a potentially important environmental risk for the persistence and dissemination of piscirickettsiosis. Piscirickettsiosis, or salmon rickettsial septicemia, is a fish disease caused by the facultative intracellular bacterium Piscirickettsia salmonis. First described in relation to the Chilean salmon farming industry 1 , this pathogen has since been reported in North America and Europe 2. A decade ago, P. salmonis was considered an obligate intracellular pathogen 3 , but later research achieved growth on artificial cell-free media 4,5. P. salmonis can survive outside of hosts for a long time as free-living cells, having been detected around salmon farms by qPCR up to 30 days after cage emptying 6 or as a biofilm mode-of-growth in a marine broth medium for 15-30 days 7. Biofilm formation is a multi-step process that involves bacterial attachment to surfaces, microcolony formation, growthdependent maturation, and cell detachment from mature biofilms to colonize new habitats 8. One persisting question is if the survival behavior of P. salmonis as a free-living bacterium is linked with a biofilm lifestyle in marine habitats. Bacterial biofilms are nearly ubiquitous in all major habitats 9 , including some synthetic habitats, such as the "plastisphere" of marine environments 10-12 .

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Section: Discussionmentioning

confidence: 99%

Improved understanding of biofilm development by Piscirickettsia salmonis reveals potential risks for the persistence and dissemination of piscirickettsiosis

Levipan

Irgang

Yáñez

et al. 2020

Sci Rep

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“…This makes mechanical removal of bacteria organized in biofilms very difficult, demonstrating greater resistance to disinfectants and antimicrobials [ 15 ]. Isiaku et al [ 16 ] and Thuptimdang et al [ 17 ] reported that biofilms play an important role in bacterial pathogenicity, especially in chronic infections where the physical and spatial arrangement of these structures impede the access of bactericidal drugs; restricting their effects to the surface, making them extraordinarily resistant to phagocytosis, and increasing the difficulty of eradicating the biofilm from their hosts [ 18 , 19 , 20 ].…”

Section: Introductionmentioning

confidence: 99%

Biofilm Produced In Vitro by Piscirickettsia salmonis Generates Differential Cytotoxicity Levels and Expression Patterns of Immune Genes in the Atlantic Salmon Cell Line SHK-1

et al. 2020

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Piscirickettsia salmonis is the causative agent of Piscirickettsiosis, an infectious disease with a high economic impact on the Chilean salmonid aquaculture industry. This bacterium produces biofilm as a potential resistance and persistence strategy against stressful environmental stimuli. However, the in vitro culture conditions that modulate biofilm formation as well as the effect of sessile bacteria on virulence and immune gene expression in host cells have not been described for P. salmonis. Therefore, this study aimed to analyze the biofilm formation by P. salmonis isolates under several NaCl and iron concentrations and to evaluate the virulence of planktonic and sessile bacteria, together with the immune gene expression induced by these bacterial conditions in an Atlantic salmon macrophage cell line. Our results showed that NaCl and Fe significantly increased biofilm production in the LF-89 type strain and EM-90-like isolates. Additionally, the planktonic EM-90 isolate and sessile LF-89 generated the highest virulence levels, associated with differential expression of il-1β, il-8, nf-κb, and iκb-α genes in SHK-1 cells. These results suggest that there is no single virulence pattern or gene expression profile induced by the planktonic or sessile condition of P. salmonis, which are dependent on each strain and bacterial condition used.

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“…These clusters of bacteria on the apical portion of the folds make us suspect biofilm formation. There are several studies on the ability of S. agalactiae to form biofilm both in vitro and in vivo (O'Toole, Kaplan, & Kolter, 2000;Randy et al 2000;Isiaku et al, 2017). There is great controversy about the influence of the environment on S. agalactiae biofilm formation, but recent studies show that low pH and the presence of nutrients such as glucose stimulate biofilm production (D'Urzo et al, 2014;Ho et al, 2013;Konto-Ghiorghi et al, 2009), similar to the conditions used in this investigation (GBS pretreated with SSF pH 5 and glucose enriched culture medium).…”

Section: Discussionmentioning

confidence: 99%

Morphological characterization of the adherence and invasion of Streptococcus agalactiae to the intestinal mucosa of tilapia Oreochromis sp.: An in vitro model

Vásquez-Machado

Barato

Iregui-Castro

2019

Journal of Fish Diseases

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Streptococcosis in tilapia Oreochromis sp. is possibly the most important bacterial disease for fish production worldwide. In Colombia, streptococcosis is caused by Streptococcus agalactiae (GBS), but in other countries, Streptococcus iniae is also involved. Prevention of streptococcosis is required and must be addressed for economic, social, international trade and public health reasons. This research used an in vitro culture of tilapia intestine to detail the intestinal mucosal response once the pathogen contacts the epithelium. We show that S. agalactiae sheds off its capsule to adhere to the epithelium. The bacterium adheres as a single individuum, in groups or in chains and is able to divide on the apical border of enterocytes. GBS adheres at and invades exclusively through the apical portion of the intestinal folds, using the transepithelial route. Once within the cytoplasm of enterocytes, the bacteria continue to divide. On the basolateral side of the epithelium, the microorganisms leave the cells to reach the propria and travel through the microcirculation. No evidence of an immuno‐inflammatory reaction or goblet cell response in the epithelium or the lamina propria was seen during the process of adherence and invasion of the pathogen.

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Biofilm is associated with chronic streptococcal meningoencephalitis in fish

Cited by 20 publications

References 52 publications

Improved understanding of biofilm development by Piscirickettsia salmonis reveals potential risks for the persistence and dissemination of piscirickettsiosis

Improved understanding of biofilm development by Piscirickettsia salmonis reveals potential risks for the persistence and dissemination of piscirickettsiosis

Biofilm Produced In Vitro by Piscirickettsia salmonis Generates Differential Cytotoxicity Levels and Expression Patterns of Immune Genes in the Atlantic Salmon Cell Line SHK-1

Morphological characterization of the adherence and invasion of Streptococcus agalactiae to the intestinal mucosa of tilapia Oreochromis sp.: An in vitro model

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