Molecular Targets for Coevolutionary Interactions Between Pacific Oyster Larvae and Their Sympatric Vibrios

Wegner, K. Mathias; Piel, Damien; Bruto, Maxime; John, Uwe; Mao, Zhijuan; Alunno‐Bruscia, Marianne; Petton, Bruno; Roux, Frédérique Le

doi:10.3389/fmicb.2019.02067

Cited by 11 publications

(9 citation statements)

References 67 publications

(109 reference statements)

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“…For example, the bacterium Aeromonas veronii, after several passages through its zebrafish host, evolved and selected for a more host-adapted derivative that was more effective at tissue migration (19). Similarly, analyses of Vibrio splendidus strains have provided evidence for allelic selection in two core genome genes that determine the bacterium's interaction with oyster larvae (32). Thus, one can envision two possible reasons for the dispersed distribution of dominant behavior seen in Fig.…”

Section: Resultsmentioning

confidence: 99%

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: Resultsmentioning

confidence: 99%

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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“…And while we have successfully identified the molecular targets of the specific host x pathogen interactions on the Vibrio pathogen side (Wegner et al, 2019), we lack an understanding of the genomic architecture of resistance of the oyster host. One of the identified Vibrio genes, OG1907 (Wegner et al, 2019) contained a Glycosyl Hydrolase 3 domain (PF00933) that could potentially be involved in modification of the complex sugar composition of the LPS (Simpson and Trent, 2019), thereby establishing a potential link to the outlier loci found here if they target galactose in LPS of Vibrio. The importance of galactose binding by C-type lectins was also reflected in the transcriptomes, where a galactose binding domain was annotated in eight differentially expressed genes.…”

Section: Discussionmentioning

confidence: 99%

“…By exploiting the specific natural history of these oyster populations, it was already shown that oysters from both invasions locally adapted to their sympatric communities of pathogenic Vibrio bacteria (Wendling and Wegner, 2015). Genomic comparisons of these Vibrio communities revealed that only few molecular targets were involved on the pathogen side (Wegner et al, 2019). While adaptive genetic divergence of oyster hosts remains unknown, these results may suggest that processes involved in the immune defense might show matching patterns of adaptive divergence.…”

Section: Introductionmentioning

confidence: 91%

Genomic and Transcriptomic Differentiation of Independent Invasions of the Pacific Oyster Crassostrea gigas

2020

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Upon colonizing new habitats, invasive species face a series of new selection pressures as a result of changing abiotic conditions and novel biotic interactions with native species. These new selection pressures can be accommodated by different mechanisms that act on different levels and across different time scales: (1) By changing transcriptomic profiles, species can react by plasticity within individual physiological limitations. (2) Invasive populations can adapt by fixing beneficial genetic variants in response to the newly encountered selection pressures. Here, we compare the genomic and transcriptomic landscapes of two independent invasions of the Pacific Oyster (Crassostrea gigas) into the North Sea. In detail, we combine ddRAD sequencing on the genomic level with RNAseq on the transcriptomic level to reveal outlier loci (SNPs) indicative of adaptation, as well as transcriptomic profiles from a translocation experiment to show immediate physiological reactions between two populations characterizing the two independent invasions. Generally, we found low physical congruence between differentially regulated genes and outlier loci, indicating that different genes are involved on the different time scales. Functionally matching outlier loci and differentially expressed genes were however found for spliceosomal modification of mRNA and particularly for transposon activation, indicating that these variation creating processes might be connected across eco-physiological and evolutionary time scales. By contrasting and identifying functional congruence between population outlier loci and population specific transcriptomic profiles, we can thus reveal a glimpse at the traits and processes characterizing specific mechanisms involved in successful invasions.

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“…Flavobacterium) [6]. Some readily culturable members of the oyster microbiome, such as strains of the Vibrio genus, have been closely studied to profile their abundance [7], pathogenic potential [8], evolution and diversity [9], and inhibition of growth by probiotics [10,11]. Other well known, cultured microbes from oysters include the protozoan pathogen Perkinsus marinus, a causative agent of Dermo disease, which is one of the major diseases of adult eastern oysters [12].…”

Section: Introductionmentioning

confidence: 99%

Diversity and Function of the Eastern Oyster (Crassostrea virginica) Microbiome

Pimentel

Dufault‐Thompson

Russo

et al. 2020

Preprint

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Marine invertebrate microbiomes play important roles in various host and ecological processes. However, a mechanistic understanding of host-microbe interactions is so far only available for a handful of model organisms. Here, an integrated taxonomic and functional analysis of the microbiome of the eastern oyster, Crassostrea virginica, was performed using 16S rRNA gene amplicon profiling, shotgun metagenomics, and genome-scale metabolic reconstruction. A relatively low number of amplicon sequence variants (ASVs) were observed in oyster tissues compared to water samples, while high variability was observed across individual oysters and among different tissue types. Targeted metagenomic sequencing of the gut microbiota led to further characterization of a dominant bacterial taxon, the class Mollicutes, which was captured by the reconstruction of a metagenome-assembled genome (MAG). Genome-scale metabolic reconstruction of the oyster Mollicutes MAG revealed a reduced set of metabolic functions and a high reliance on the uptake of host-derived nutrients. A chitin degradation and an arginine deiminase pathway were unique to the MAG as compared to other closely related Mycoplasma genomes, indicating a distinct mechanism of carbon and energy acquisition by the oyster- associated Mollicutes. A systematic reanalysis of public eastern oyster-derived microbiome data revealed the Mollicutes as a ubiquitous taxon among adult oysters despite their general absence in larvae and biodeposit samples, suggesting potential horizontal transmission via an unknown mechanism.IMPORTANCEDespite well-documented biological significance of invertebrate microbiomes, a detailed taxonomic and functional characterization is frequently missing from many non-model marine invertebrates. By using 16S rRNA gene-based community profiling, shotgun metagenomics, and genome-scale metabolic reconstruction, this study provides an integrated taxonomic and functional analysis of the microbiome of the eastern oyster, Crassostrea virginica. Community profiling revealed a surprisingly low richness, as compared to surrounding seawater, and high variability among different tissue types and individuals. Reconstruction of a Mollicutes MAG enabled the phylogenomic positioning and functional characterization of the oyster-associated Mollicutes. Comparative analysis of the adult oyster gut, biodeposits, and oyster larvae samples indicated the potentially ubiquitous associations of the Mollicutes taxon with adult oysters. To the best of our knowledge, this study represented the first metagenomics derived functional inference of the eastern oyster microbiome. An integrated analytical procedure was developed for the functional characterization of microbiomes in other non-model host species.

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Molecular Targets for Coevolutionary Interactions Between Pacific Oyster Larvae and Their Sympatric Vibrios

Cited by 11 publications

References 67 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

Genomic and Transcriptomic Differentiation of Independent Invasions of the Pacific Oyster Crassostrea gigas

Diversity and Function of the Eastern Oyster (Crassostrea virginica) Microbiome

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