Comparative Genome Analyses of
            <i>Vibrio anguillarum</i>
            Strains Reveal a Link with Pathogenicity Traits

Castillo, Daniel; Alvise, Paul D.; Xu, Ruiqi; Zhang, Faxing; Middelboe, Mathias; Gram, Lone

doi:10.1128/msystems.00001-17

Cited by 51 publications

(76 citation statements)

References 93 publications

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“…Interestingly, while the number of strains was insufficient to perform a robust statistical analysis, we noticed that although some strains with the same behavior clustered, others were spread across the tree; i.e., there is no obvious relationship between genome-wide phylogeny and behavior. Nevertheless, at the tips of the phylogenetic tree, there is some evidence of clustering of symbionts having the same colonization behavior, as has been found for the phylogenetic clustering of the degree of virulence of strains of the fish pathogen Vibrio anguillarum (28). The latter work also suggested a geographic association between similar strains, which we did not see.…”

Section: Resultssupporting

confidence: 65%

Using Colonization Assays and Comparative Genomics To Discover Symbiosis Behaviors and Factors in Vibrio fischeri

Bongrand

Moriano‐Gutierrez

Arevalo

et al. 2020

mBio

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The luminous marine Gram-negative bacterium Vibrio (Aliivibrio) fischeri is the natural light organ symbiont of several squid species, including the Hawaiian bobtail squid, Euprymna scolopes, and the Japanese bobtail squid, Euprymna morsei. Work with E. scolopes has shown how the bacteria establish their niche in the light organ of the newly hatched host. Two types of V. fischeri strains have been distinguished based upon their behavior in cocolonization competition assays in juvenile E. scolopes, i.e., (i) niche-sharing or (ii) niche-dominant behavior. This study aimed to determine whether these behaviors are observed with other V. fischeri strains or whether they are specific to those isolated from E. scolopes light organs. Cocolonization competition assays between V. fischeri strains isolated from the congeneric squid E. morsei or from other marine animals revealed the same sharing or dominant behaviors. In addition, whole-genome sequencing of these strains showed that the dominant behavior is polyphyletic and not associated with the presence or absence of a single gene or genes. Comparative genomics of 44 squid light organ isolates from around the globe led to the identification of symbiosis-specific candidates in the genomes of these strains. Colonization assays using genetic derivatives with deletions of these candidates established the importance of two such genes in colonization. This study has allowed us to expand the concept of distinct colonization behaviors to strains isolated from a number of squid and fish hosts. IMPORTANCE There is an increasing recognition of the importance of strain differences in the ecology of a symbiotic bacterial species and, in particular, how these differences underlie crucial interactions with their host. Nevertheless, little is known about the genetic bases for these differences, how they manifest themselves in specific behaviors, and their distribution among symbionts of different host species. In this study, we sequenced the genomes of Vibrio fischeri isolated from the tissues of squids and fishes and applied comparative genomics approaches to look for patterns between symbiont lineages and host colonization behavior. In addition, we identified the only two genes that were exclusively present in all V. fischeri strains isolated from the light organs of sepiolid squid species. Mutational studies of these genes indicated that they both played a role in colonization of the squid light organ, emphasizing the value of applying a comparative genomics approach in the study of symbioses.

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Section: Resultssupporting

confidence: 65%

Using Colonization Assays and Comparative Genomics To Discover Symbiosis Behaviors and Factors in Vibrio fischeri

Bongrand

Moriano‐Gutierrez

Arevalo

et al. 2020

mBio

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“…For instance, two phages VfO4K68 and VfO3K6 that carry the zona occludens toxin (Zot) and the accessory cholera enterotoxin (Ace), have been isolated from V. parahaemolyticus (4, 5). Zot and Ace are particularly common among vibriophages isolated from human pathogens, such as V. cholerae and V. parahaemolyticus (6-8) but are also present in prophage-like elements of non-human pathogens such as V. coralliilyticus (9) and V. anguillarum (10), suggesting frequent HGT among different vibrio species (11).…”

Section: Introductionmentioning

confidence: 99%

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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“…Strains PMA 2.15 and PMA 3.15 harbored GIs (#9, #12) that encode genes related to biosynthesis and modification of LPS ( Figure 4A ). The existence of these accessory genes is regarded as an essential virulence factor in Burkholderia pseudomallei ( Reckseidler et al, 2001 ), V. anguillarum ( Castillo et al, 2017 ), and V. cholerae ( Chun et al, 2009 ). More importantly, the presence of these genes has been linked to the modification of capsule polysaccharide content, adherence and evasion of the immune system ( Sim et al, 2010 ).…”

Section: Discussionmentioning

confidence: 99%

“…Also, the highly cytotoxic strains PMC 53.7, PMA 2.15, and PMA 3.15 harbored a prophage-like element encoding a Zot toxin ( Figure 4B ), which has been described previously in V. cholerae as a second toxin ( Waldor and Mekalanos, 1996 ) whose function increases intestinal permeability by interacting with a mammalian cell receptor with subsequent activation of intracellular signaling leading to disassembly of the intercellular tight junctions ( Di Pierro et al, 2001 ; Marinaro et al, 2003 ). It has also been found in prophage-like elements in V. coralliilyticus ( Weynberg et al, 2016 ) and V. anguillarum ( Castillo et al, 2017 ), suggesting that the occurrence and exchange of prophages encoding zot -like toxins is frequent in Vibrio communities. The Zot-like toxin found in strain PMA 2.15 was similar to the toxin encoded in prophage f237 from the pandemic V. parahaemolyticus strains belonging to the O3:K6 serovar ( Nasu et al, 2000 ).…”

Section: Discussionmentioning

confidence: 99%

Exploring the Genomic Traits of Non-toxigenic Vibrio parahaemolyticus Strains Isolated in Southern Chile

et al. 2018

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Vibrio parahaemolyticus is the leading cause of seafood-borne gastroenteritis worldwide. As reported in other countries, after the rise and fall of the pandemic strain in Chile, other post-pandemic strains have been associated with clinical cases, including strains lacking the major toxins TDH and TRH. Since the presence or absence of tdh and trh genes has been used for diagnostic purposes and as a proxy of the virulence of V. parahaemolyticus isolates, the understanding of virulence in V. parahaemolyticus strains lacking toxins is essential to detect these strains present in water and marine products to avoid possible food-borne infection. In this study, we characterized the genome of four environmental and two clinical non-toxigenic strains (tdh-, trh-, and T3SS2-). Using whole-genome sequencing, phylogenetic, and comparative genome analysis, we identified the core and pan-genome of V. parahaemolyticus of strains of southern Chile. The phylogenetic tree based on the core genome showed low genetic diversity but the analysis of the pan-genome revealed that all strains harbored genomic islands carrying diverse virulence and fitness factors or prophage-like elements that encode toxins like Zot and RTX. Interestingly, the three strains carrying Zot-like toxin have a different sequence, although the alignment showed some conserved areas with the zot sequence found in V. cholerae. In addition, we identified an unexpected diversity in the genetic architecture of the T3SS1 gene cluster and the presence of the T3SS2 gene cluster in a non-pandemic environmental strain. Our study sheds light on the diversity of V. parahaemolyticus strains from the southern Pacific which increases our current knowledge regarding the global diversity of this organism.

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Comparative Genome Analyses of Vibrio anguillarum Strains Reveal a Link with Pathogenicity Traits

Cited by 51 publications

References 93 publications

Using Colonization Assays and Comparative Genomics To Discover Symbiosis Behaviors and Factors in Vibrio fischeri

Using Colonization Assays and Comparative Genomics To Discover Symbiosis Behaviors and Factors in Vibrio fischeri

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

Exploring the Genomic Traits of Non-toxigenic Vibrio parahaemolyticus Strains Isolated in Southern Chile

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