Dataset Information

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.

ABSTRACT: Microbiota provide their hosts with a range of beneficial services, including defense from external pathogens. However, host-associated microbial communities themselves can act as a source of opportunistic pathogens depending on the environment. Marine poikilotherms and their microbiota are strongly influenced by temperature, but experimental studies exploring how temperature affects the interactions between both parties are rare. To assess the effects of temperature, temperature stress and infection on diversity, composition and dynamics of the hemolymph microbiota of Pacific oysters (Crassostrea gigas), we conducted an experiment in a fully-crossed, three-factorial design, in which the temperature acclimated oysters (8 or 22?°C) were exposed to temperature stress and to experimental challenge with a virulent Vibrio sp. strain. We monitored oyster survival and repeatedly collected hemolymph of dead and alive animals to determine the microbiome composition by 16s rRNA gene amplicon pyrosequencing. We found that the microbial dynamics and composition of communities in healthy animals (including infection survivors) were significantly affected by temperature and temperature stress, but not by infection. The response was mediated by changes in the incidence and abundance of operational taxonomic units (OTUs) and accompanied by little change at higher taxonomic levels, indicating dynamic stability of the hemolymph microbiome. Dead and moribund oysters, on the contrary, displayed signs of community structure disruption, characterized by very low diversity and proliferation of few OTUs. We can therefore link short-term responses of host-associated microbial communities to abiotic and biotic factors and assess the potential feedback between microbiota dynamics and host survival during disease.

SUBMITTER: Lokmer A

PROVIDER: S-EPMC4331581 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.

Lokmer Ana A Mathias Wegner Karl K

The ISME journal 20140902 3

Microbiota provide their hosts with a range of beneficial services, including defense from external pathogens. However, host-associated microbial communities themselves can act as a source of opportunistic pathogens depending on the environment. Marine poikilotherms and their microbiota are strongly influenced by temperature, but experimental studies exploring how temperature affects the interactions between both parties are rare. To assess the effects of temperature, temperature stress and infe ...[more]

PMID: 25180968

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Project description:Vibrio aestuarianus is a bacterium related to mortality outbreaks in Pacific oysters, Crassostrea gigas, in France, Ireland, and Scotland since 2011. Knowledge about its transmission dynamics is still lacking, impairing guidance to prevent and control the related disease spread. Mathematical modeling is a relevant approach to better understand the determinants of a disease and predict its dynamics in imperfectly observed pathosystems. We developed here the first marine epidemiological model to estimate the key parameters of V. aestuarianus infection at a local scale in a small and closed oyster population under controlled laboratory conditions. Using a compartmental model accounting for free-living bacteria in seawater, we predicted the infection dynamics using dedicated and model-driven collected laboratory experimental transmission data. We estimated parameters and showed that waterborne transmission of V. aestuarianus is possible under experimental conditions, with a basic reproduction number R0 of 2.88 (95% CI: 1.86; 3.35), and a generation time of 5.5 days. Our results highlighted a bacterial dose-dependent transmission of vibriosis at local scale. Global sensitivity analyses indicated that the bacteria shedding rate, the concentration of bacteria in seawater that yields a 50% chance of catching the infection, and the initial bacterial exposure dose W0 were three critical parameters explaining most of the variation in the selected model outputs related to disease spread, i.e., R0, the maximum prevalence, oyster survival curve, and bacteria concentration in seawater. Prevention and control should target the exposure of oysters to bacterial concentration in seawater. This combined laboratory-modeling approach enabled us to maximize the use of information obtained through experiments. The identified key epidemiological parameters should be better refined by further dedicated laboratory experiments. These results revealed the importance of multidisciplinary approaches to gain consistent insights into the marine epidemiology of oyster diseases.

Project description:Summer mortality of Crassostrea gigas is the result of a complex interaction between oysters, their environment and pathogens. A large genetic basis and a high heritability were demonstrated for the observed variation in resistance to summer mortality, which offered the possibility to develop lines of oysters that were resistant (R) or susceptible (S) to summer mortality. Previously, genome-wide expression profiling of R and S oyster gonads highlighted reproduction and antioxidant defense as constitutive pathways that operate differentially between these two lines. Here, we show that signaling in innate immunity also operates differentially between these lines and we postulated that it is at the main origin of their difference of survival in the field. From the already published microarray data, we employed an ANOVA analysis that reveals a specific “immune” profile at the date preceding the mortality. In addition, we conducted a microarray profiling of two other tissues, gills and muscle, that also showed an over-representation of the immune genes (46%) among the selected genes. Eleven genes were pinpointed to be simultaneously differentially expressed between R and S lines in the three tissues. Among them, ten are related to “Immune Response”. The kinetics of their mRNA levels appeared clearly different between lines and suggests that in environment, R oysters had the capacity to modulate signaling in innate immunity whereas S oysters did not. This study enhances our understanding of the complex summer mortality syndrome and provides candidates of interest for further functional and genetics studies. For microarray analysis, R and S oysters were sampled three times (dates 1 to 3: May 25, June 6, and June 20, respectively). On each date, 3 replicates of 8 oysters were sampled from each line (R and S) for three tissues (gonad, muscle and fills) and all the samples prepared for total RNA extraction. Furthermore, the entire tissues of 10 wild oysters were collected, pooled and homogenized to constitute a single total RNA sample for use as a reference in all slide hybridizations and RT-PCR analysis. For microarray hybridizations, 5µg of total RNA were directly labeled by reverse transcription and then purified using the Direct ShipShot Labeling kit (Promega). This reaction was performed for each of the 18 samples, with Cy5 (red) incorporation. The reference sample was Cy3-labeled (green) in 18 separate tubes following the same protocol. The 18 Cy3-labeled cDNAs were next pooled, and then divided once more into 18 samples to obtain a homogeneous reference. Equimolar amounts of cDNA samples and cDNA reference labeled with Cy5 and Cy3, respectively, were SpeedVac evaporated and mixed into a single pool with the hybridization buffer (ChipHyb™ hybridization buffer, Ventana Discovery, Tucson, AZ, USA). They were then co-hybridized on the same microarray slide, in a Ventana hybridization station (Ventana Discovery, Tucson, AZ, USA). The data submitted here correspond to the mean of the three replicates for each line and each date, representing 18 samples.

Dataset Information

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.

Publications

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.

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