Prevalence of genetically similar <i>Flavobacterium columnare</i> phages across aquaculture environments reveals a strong potential for pathogen control

Runtuvuori-Salmela, Anniina; Kunttu, H.M.T.; Laanto, Elina; Almeida, Gabriel Marchesan; Mäkelä, Kati; Middelboe, Mathias; Sundberg, Lotta‐Riina

doi:10.1111/1462-2920.15901

Cited by 7 publications

(7 citation statements)

References 78 publications

(117 reference statements)

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“…Interestingly, isolates exposed to FCL-2 did not have mutations in gliding motility related genes, suggesting that FCL-2 uses other receptors for infection of F. columnare than the other phages. FCL-2 differs genetically from other phages infecting genetic group G bacteria (This article was submitted to an online preprint archive [36]), supporting this suggestion.…”

Section: Discussionmentioning

confidence: 71%

“…Bacteria and phages used in this study were isolated from water samples collected from fish farms during columnaris outbreaks (This article was submitted to an online preprint archive [36]) (Table 5). Bacteria were confirmed as F. columnare by restriction fragment length polymorphism (RFLP) analysis of 16S rRNA gene and classified into genetic groups by RFLP of 16S-23S internal transcribed spacer (ITS) region (This article was submitted to an online preprint archive [36]). All the six phages belong to the Myoviridae family and have been characterised with respect to host range and genomic composition (This article was submitted to an online preprint archive [36]).…”

Section: Bacterial and Phage Isolatesmentioning

confidence: 99%

“…Bacteria were confirmed as F. columnare by restriction fragment length polymorphism (RFLP) analysis of 16S rRNA gene and classified into genetic groups by RFLP of 16S-23S internal transcribed spacer (ITS) region (This article was submitted to an online preprint archive [36]). All the six phages belong to the Myoviridae family and have been characterised with respect to host range and genomic composition (This article was submitted to an online preprint archive [36]).…”

Section: Bacterial and Phage Isolatesmentioning

confidence: 99%

“…Two phage-sensitive wild-type F. columnare isolates, the high-virulence FCO-F2 isolate (genetic group C) and the medium-virulence FCO-F9 isolate (genetic group G) (This article was submitted to an online preprint archive [36]), were each exposed to three phages in separate experiments with individual phages. Isolate FCO-F2 was exposed to phages FCOV-F2, FCOV-F5 and FCOV-F25, and isolate FCO-F9 to phages FCL-2, FCOV-F13 and FCOV-F45, in accordance with the host range of the phages.…”

Section: Phage Exposure Experiments and Isolation Of Coloniesmentioning

confidence: 99%

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Bacteriophage Resistance Affects Flavobacterium columnare Virulence Partly via Mutations in Genes Related to Gliding Motility and the Type IX Secretion System

Kunttu

Runtuvuori-Salmela

Sundell

et al. 2021

Appl Environ Microbiol

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Increasing problems with antibiotic resistance has directed interest towards phage therapy in the aquaculture industry. However, phage resistance evolving in target bacteria is considered a challenge. To investigate how phage resistance influences the fish pathogen Flavobacterium columnare , two wild-type bacterial isolates, FCO-F2 and FCO-F9, were exposed to phages (FCO-F2 to FCOV-F2, FCOV-F5 and FCOV-F25, and FCO-F9 to FCL-2, FCOV-F13 and FCOV-F45), and resulting phenotypic and genetic changes in bacteria were analyzed. Bacterial viability first decreased in the exposure cultures, but started to increase after 1-2 days, along with a change in colony morphology from original rhizoid to rough, leading to 98% prevalence of the rough morphotype. Twenty-four isolates (including four isolates from no-phage treatments) were further characterized for phage resistance, antibiotic susceptibility, motility, adhesion and biofilm formation, protease activity, whole genome sequencing and virulence in rainbow trout fry. The rough isolates arising in phage exposure were phage-resistant with low virulence, whereas rhizoid isolates maintained phage susceptibility and high virulence. Gliding motility and protease activity were also related to the phage susceptibility. Observed mutations in phage-resistant isolates were mostly located in genes coding for type IX secretion system, a component of the Bacteroidetes gliding motility machinery. However, not all phage-resistant isolates had mutations, indicating that phage resistance in F. columnare is a multifactorial process including both genetic mutations and changes in gene expression. Phage resistance may not, however, be a challenge for development of phage therapy against F. columnare infections, since phage resistance is associated with decrease in bacterial virulence. Importance Phage resistance of infectious bacteria is a common phenomenon posing challenges for development of phage therapy. Along with growing world population and need for increased food production, constantly intensifying animal farming has to face increasing problems of infectious diseases. Columnaris disease, caused by F. columnare , is a worldwide threat for salmonid fry and juvenile farming. Without antibiotic treatments, infections can lead to 100% mortality in a fish stock. Phage therapy of columnaris disease would reduce a development of antibiotic-resistant bacteria and antibiotic loads by the aquaculture industry, but phage-resistant bacterial isolates may become a risk. However, phenotypic and genetic characterization of phage-resistant F. columnare isolates in this study revealed that they are less virulent than phage-susceptible isolates and thus not a challenge for phage therapy against columnaris disease. This is a valuable information for the fish farming industry globally when considering phage-based prevention and curing methods for F. columnare infections.

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Section: Discussionmentioning

confidence: 71%

Section: Bacterial and Phage Isolatesmentioning

confidence: 99%

Section: Bacterial and Phage Isolatesmentioning

confidence: 99%

Section: Phage Exposure Experiments and Isolation Of Coloniesmentioning

confidence: 99%

See 2 more Smart Citations

Bacteriophage Resistance Affects Flavobacterium columnare Virulence Partly via Mutations in Genes Related to Gliding Motility and the Type IX Secretion System

Kunttu

Runtuvuori-Salmela

Sundell

et al. 2021

Appl Environ Microbiol

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“…The dominance, in the environment, of one, or few, genera of phages infective to a certain bacterial host species has been reported previously. Recent examples relevant to agriculture are the prevalence of Limestoneviruses among phages infecting potato pathogen Dickeya solani [ 82 , 83 ], and Ficleduoviruses among phages of aquaculture pathogen Flavobacterium columnare [ 84 ]. The accumulation of statistically robust data on available phage diversity either takes decades (as for E. coli or Pseudomonas sp.…”

Section: Discussionmentioning

confidence: 99%

Prophage-Derived Regions in Curtobacterium Genomes: Good Things, Small Packages

Evseev

Lukianova

Tarakanov

et al. 2023

IJMS

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Curtobacterium is a genus of Gram-positive bacteria within the order Actinomycetales. Some Curtobacterium species (C. flaccumfaciens, C. plantarum) are harmful pathogens of agricultural crops such as soybean, dry beans, peas, sugar beet and beetroot, which occur throughout the world. Bacteriophages (bacterial viruses) are considered to be potential curative agents to control the spread of harmful bacteria. Temperate bacteriophages integrate their genomes into bacterial chromosomes (prophages), sometimes substantially influencing bacterial lifestyle and pathogenicity. About 200 publicly available genomes of Curtobacterium species, including environmental metagenomic sequences, were inspected for the presence of sequences of possible prophage origin using bioinformatic methods. The comparison of the search results with several ubiquitous bacterial groups showed the relatively low level of the presence of prophage traces in Curtobacterium genomes. Genomic and phylogenetic analyses were undertaken for the evaluation of the evolutionary and taxonomic positioning of predicted prophages. The analyses indicated the relatedness of Curtobacterium prophage-derived sequences with temperate actinophages of siphoviral morphology. In most cases, the predicted prophages can represent novel phage taxa not described previously. One of the predicted temperate phages was induced from the Curtobacterium genome. Bioinformatic analysis of the modelled proteins encoded in prophage-derived regions led to the discovery of some 100 putative glycopolymer-degrading enzymes that contained enzymatic domains with predicted cell-wall- and cell-envelope-degrading activity; these included glycosidases and peptidases. These proteins can be considered for the experimental design of new antibacterials against Curtobacterium phytopathogens.

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