Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities

Castillo, Daniel; Kauffman, Kathryn M.; Hussain, Fatima A.; Kalatzis, Panos G.; Rørbo, Nanna; Polz, Martin F.; Middelboe, Mathias

doi:10.1038/s41598-018-28326-9

Cited by 90 publications

(99 citation statements)

References 45 publications

(68 reference statements)

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“…Many vibriophages contain virulence genes responsible for severe gastro-intestinal diseases (47, 48). For instance, almost 80% of clinical V. parahaemolyticus strains contain filamentous phages, encoding the zona occludens toxin (Zot) (22). Also, non-human pathogens, such as V. coralliilyticus and V. anguillarum contain prophage-like elements encoding Zot, suggesting frequent horizontal gene transfer (HGT) of Zot via prophages among vibrios (11).…”

Section: Discussionmentioning

confidence: 99%

“…We predict, that also filamentous phages isolated from environmental vibrios, may contain virulence factors responsible for disease outbreaks in marine eukaryotes. Indeed, a closer look at more than 1,800 Vibrio genome sequences, covering 64 species revealed that 45% harboured filamentous phages which encoded Zot-like proteins (22). Even though a detailed characterization of these phages is missing, this study suggests that also filamentous vibriophages of non-human pathogens contain virulence genes in (22).…”

Section: Introductionmentioning

confidence: 99%

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Closely relatedVibrio alginolyticusstrains encode an identical repertoire of prophages and filamentous phages

Chibani

Hertel

Hoppert

et al. 2019

Preprint

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Filamentous vibriophages represent a massive repertoire of virulence factors which can be transferred across species boundaries, leading to the emergence of deadly pathogens. All filamentous vibriophages that were characterized until today were isolated from human pathogens. Considering frequent horizontal gene transfer among vibrios, we predict that other environmental isolates, including non-human pathogens also carry filamentous phages, of which some may encode virulence factors.The aim of this study was to characterize the phage repertoire, consisting of prophages and filamentous phages, of a marine pathogen, Vibrio alginolyticus. To do so, we sequenced eight different V. alginolyticus strains, isolated from different pipefish and characterised their phage repertoire using a combination of morphological analyses and comparative genomics.We were able to identify a total of five novel phage regions (three different Caudovirales and two different Inoviridae), whereby only those two loci predicted to correspond to filamentous phages (family Inoviridae) represent actively replicating phages. Unique for this study was that all eight host strains, which were isolated from different eukaryotic hosts have identical bacteriophages, suggesting a clonal expansion of this strain after the phages had been acquired by a common ancestor. We further found that co-occurrence of two different filamentous phages leads to within-host competition resulting in reduced phage replication by one of the two phages. One of the two filamentous phages encoded two virulence genes (Ace and Zot), homologous to those encoded on the V. cholerae phage CTXΦ. The coverage of these zot-encoding phages correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phages is an important virulence determinant.Impact statementMany bacteria of the genus Vibrio, such as V. cholerae or V. parahaemolyticus impose a strong threat to human health. Often, small viruses, known as filamentous phages encode virulence genes. Upon infecting a bacterial cell, these phages can transform a previously harmless bacterium into a deadly pathogen. While filamentous phages and their virulence factors are well-characterized for human pathogenic vibrios, filamentous phages of marine vibrios, pathogenic for a wide range of marine organisms, are predicted to carry virulence factors, but have so far not been characterized in depth. Using whole genome sequencing and comparative genomics of phages isolated from a marine fish pathogen V. alginolyticus, we show that also environmental strains harbour filamentous phages that carry virulence genes. These phages were most likely acquired from other vibrios by a process known as horizontal gene transfer. We found that these phages are identical across eight different pathogenic V. alginolyticus strains, suggesting that they have been acquired by a common ancestor before a clonal expansion of this ecotype took place. The phages characterized in this study have not been described before and are unique for the Kiel V. alginolyticus ecotype.Data SummaryThe GenBank accession numbers for all genomic sequence data analysed in the present study can be found in Table S1.All phage regions identified by PHASTER analysis of each chromosome and the respective coverage of active phage loci are listed in Table S2.GenBank files were deposited at NCBI for the two actively replicating filamentous phages VALGΦ6 (Accession number: MN719123) and VALGΦ8 (Accession number: MN690600)The virulence data from the infection experiments have been deposited at PANGAEA: Accession number will be provided upon acceptance of the manuscript.Data statementAll supporting data have been provided within the article or through supplementary data files. Four supplementary tables and six supplementary figures are available with the online version of this article.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Closely relatedVibrio alginolyticusstrains encode an identical repertoire of prophages and filamentous phages

Chibani

Hertel

Hoppert

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Similarly, Castillo et al. () revealed that the prophage‐like elements encoding possible virulence and antibiotic resistance are widely distributed among the 64 species of environmental vibrios, including those classified as nonpathogenic.…”

Section: Transmission and Virulence Factors Influencing Vibriosismentioning

confidence: 97%

“…; Castillo et al. ), while integration of genomic and phenotypic features enlightens the molecular evolution of the pathogenic Vibrio spp. (Castillo et al.…”

Section: Potential Control and Prevention Measures Against Vibriosismentioning

confidence: 99%

Vibriosis in Fish: A Review on Disease Development and Prevention

et al. 2018

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Current growth in aquaculture production is parallel with the increasing number of disease outbreaks, which negatively affect the production, profitability, and sustainability of the global aquaculture industry. Vibriosis is among the most common diseases leading to massive mortality of cultured shrimp, fish, and shellfish in Asia. High incidence of vibriosis can occur in hatchery and grow-out facilities, but juveniles are more susceptible to the disease. Various factors, particularly the source of fish, environmental factors (including water quality and farm management), and the virulence factors of Vibrio, influence the occurrence of the disease . Affected fish show weariness, with necrosis of skin and appendages, leading to body malformation, slow growth, internal organ liquefaction, blindness, muscle opacity, and mortality. A combination of control measures, particularly a disease-free source of fish, biosecurity of the farm, improved water quality, and other preventive measures (e.g., vaccination) might be able to control the infection. Although some control measures are expensive and less practical, vaccination is effective, relatively cheap, and easily implemented. In this review, the latest knowledge on the pathogenesis and control of vibriosis, including vaccination, is discussed. 4INA-SALWANY ET AL.

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“…Recent assessment of prophages in diverse marine populations of Vibrio spp. suggests that filamentous prophages are numerous and widespread and play comprehensive roles in evolution through shaping niche adaptation and emergence of novel pathogenic strains emerging from environmental Vibrio communities . Recently, a prophage with a similar genomic arrangement to CTXφ has been described in the human pathogen Acinetobacter baylyi (and A. baumannii ) genome, though no homologous CTX toxin is present .…”

Section: Escherichia Coli Ff: the Archetypal Filamentous Phagementioning

confidence: 99%

Filamentous phages: masters of a microbial sharing economy

2019

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Bacteriophage (“bacteria eaters”) or phage is the collective term for viruses that infect bacteria. While most phages are pathogens that kill their bacterial hosts, the filamentous phages of the sub‐class Inoviridae live in cooperative relationships with their bacterial hosts, akin to the principal behaviours found in the modern‐day sharing economy: peer‐to‐peer support, to offset any burden. Filamentous phages impose very little burden on bacteria and offset this by providing service to help build better biofilms, or provision of toxins and other factors that increase virulence, or modified behaviours that provide novel motile activity to their bacterial hosts. Past, present and future biotechnology applications have been built on this phage–host cooperativity, including DNA sequencing technology, tools for genetic engineering and molecular analysis of gene expression and protein production, and phage‐display technologies for screening protein–ligand and protein–protein interactions. With the explosion of genome and metagenome sequencing surveys around the world, we are coming to realize that our knowledge of filamentous phage diversity remains at a tip‐of‐the‐iceberg stage, promising that new biology and biotechnology are soon to come.

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Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities

Cited by 90 publications

References 45 publications

Closely relatedVibrio alginolyticusstrains encode an identical repertoire of prophages and filamentous phages

Closely relatedVibrio alginolyticusstrains encode an identical repertoire of prophages and filamentous phages

Vibriosis in Fish: A Review on Disease Development and Prevention

Filamentous phages: masters of a microbial sharing economy

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