Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria

Wendling, Carolin Charlotte; Piecyk, Agnes; Refardt, Dominik; Chibani, Cynthia Maria; Hertel, Robert; Liesegang, Heiko; Bunk, Boyke; Overmann, Jörg; Roth, Olivia

doi:10.1186/s12862-017-0930-2

Cited by 34 publications

(74 citation statements)

References 61 publications

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“…In concert with this comparative approach, experimental (although see Ref. [72]) and theoretical (although see Ref. [73]) work will be required to unpick the ecology and evolution of these complex and intriguing interactions at finer scales.…”

Section: Discussionmentioning

confidence: 99%

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

2017

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Infection by a temperate phage can lead to death of the bacterial cell, but sometimes these phages integrate into the bacterial chromosome, offering the potential for a more long-lasting relationship to be established. Here we define three major ecological and evolutionary benefits of temperate phage for bacteria: as agents of horizontal gene transfer (HGT), as sources of genetic variation for evolutionary innovation, and as weapons of bacterial competition. We suggest that a coevolutionary perspective is required to understand the roles of temperate phages in bacterial populations.

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Section: Discussionmentioning

confidence: 99%

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

2017

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“…Vibrio alginolyticus strains used in the present study were isolated either from the gut or the gills of six different pipefish ( Syngnathus typhle ) in the Kiel Fjord in 2012 (27) and have been shown to cause mortality in juvenile pipefish ((28), and this study). Using a combination of PacBio and Illumina sequencing we generated eight closed bacterial genomes of the host bacteria as described in (28).…”

Section: Methodsmentioning

confidence: 99%

“…We induced filamentous phages from all nine V. alginolyticus strains using Mitomycin C (Sigma), for details see (28), with some modifications: bacteria were grown in liquid Medium101 (Medium101: 0.5% (w/v) peptone, 0.3% (w/v) meat extract, 3.0% (w/v) NaCl in MilliQ water) at 250 rpm and 25 °C overnight. Cultures were diluted 1:100 in fresh medium at a total volume of 20ml and grown for another 2h at 250 rpm and 25 °C to bring cultures into exponential growth before adding Mitomycin C at a final concentration of 0.5 μg/ml.…”

Section: Methodsmentioning

confidence: 99%

“…We performed a controlled infection experiment to estimate the virulence of the eight sequenced strains on juvenile pipefish (a detailed description of methods and the statistical analysis can be found in (28). Briefly, we fed 9-12 juvenile pipefish per tank in using triplicate tanks with Artemia nauplii which were previously exposed to ∼10 9 CFU/ml or seawater as control.…”

Section: Methodsmentioning

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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“…We are aware that with the use of sympatric Vibrio strains, we would likely obtain different results, as closely related Vibrio strains may cover a broad range of virulence (Wendling et al. , in revision). However, our experimental design did not permit the testing of multiple Vibrio strains.…”

Section: Methodsmentioning

confidence: 99%

Selection by higher‐order effects of salinity and bacteria on early life‐stages of Western Baltic spring‐spawning herring

Poirier

Listmann

Roth

2017

Evolutionary Applications

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Habitat stratification by abiotic and biotic factors initiates divergence of populations and leads to ecological speciation. In contrast to fully marine waters, the Baltic Sea is stratified by a salinity gradient that strongly affects fish physiology, distribution, diversity and virulence of important marine pathogens. Animals thus face the challenge to simultaneously adapt to the concurrent salinity and cope with the selection imposed by the changing pathogenic virulence. Western Baltic spring‐spawning herring (Clupea harengus) migrate to spawning grounds characterized by different salinities to which herring are supposedly adapted. We hypothesized that herring populations do not only have to cope with different salinity levels but that they are simultaneously exposed to higher‐order effects that accompany the shifts in salinity, that is induced pathogenicity of Vibrio bacteria in lower saline waters. To experimentally evaluate this, adults of two populations were caught in their spawning grounds and fully reciprocally crossed within and between populations. Larvae were reared at three salinity levels, representing the spawning ground salinity of each of the two populations, or Atlantic salinity conditions resembling the phylogenetic origin of Clupea harengus. In addition, larvae were exposed to a Vibrio spp. infection. Life‐history traits and gene expression analysis served as response variables. Herring seem adapted to Baltic Sea conditions and cope better with low saline waters. However, upon a bacterial infection, herring larvae suffer more when kept at lower salinities implying reduced resistance against Vibrio or higher Vibrio virulence. In the context of recent climate change with less saline marine waters in the Baltic Sea, such interactions may constitute key future stressors.

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Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria

Cited by 34 publications

References 61 publications

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

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

Selection by higher‐order effects of salinity and bacteria on early life‐stages of Western Baltic spring‐spawning herring

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