Host-microbiota-parasite interactions in two wild sparid fish species, Diplodus annularis and Oblada melanura (Teleostei, Sparidae) over a year: a pilot study.

BACKGROUND: The microbiota in fish external mucus is mainly known for having a role in homeostasis and protection against pathogens, but recent evidence suggests it is also involved in the host-specificity of some ectoparasites. In this study, we investigated the influence of seasonality and environmental factors on both fish external microbiota and monogenean gill ectoparasites abundance and diversity and assessed the level of covariations between monogenean and bacterial communities across seasons. To do so, we assessed skin and gill microbiota of two sparid species, Oblada melanura and Diplodus annularis, over a year and collected their specific monogenean ectoparasites belonging to the Lamellodiscus genus. RESULTS: Our results revealed that diversity and structure of skin and gill mucus microbiota were strongly affected by seasonality, mainly by the variations of temperature, with specific fish-associated bacterial taxa for each season. The diversity and abundance of parasites were also influenced by seasonality, with the abundance of some Lamellodiscus species significantly correlated to temperature. Numerous positive and negative correlations between the abundance of given bacterial genera and Lamellodiscus species were observed throughout the year, suggesting their differential interaction across seasons. CONCLUSIONS: The present study is one of the first to demonstrate the influence of seasonality and related abiotic factors on fish external microbiota over a year. We further identified potential interactions between gill microbiota and parasite occurrence in wild fish populations, improving current knowledge and understanding of the establishment of host-specificity.

Many parasitoids lack adult fat accumulation, despite fatty acid synthesis: A discussion of concepts and considerations for future research.

Fat reserves, specifically the accumulation of triacylglycerols, are a major energy source and play a key role for life histories. Fat accumulation is a conserved metabolic pattern across most insects, yet in most parasitoid species adults do not gain fat mass, even when nutrients are readily available and provided ad libitum. This extraordinary physiological phenotype has evolved repeatedly in phylogenetically dispersed parasitoid species. This poses a conundrum because it could lead to significant constraints on energy allocation toward key adult functions such as survival and reproduction. Recent work on the underlying genetic and biochemical mechanisms has spurred a debate on fat accumulation versus fat production, because of incongruent interpretation of results obtained using different methodologies. This debate is in part due to semantics, highlighting the need for a synthetic perspective on fat accumulation that reconciles previous debates and provides new insights and terminology. In this paper, we propose updated, unambiguous terminology for future research in the field, including "fatty acid synthesis" and "lack of adult fat accumulation", and describe the distinct metabolic pathways involved in the complex process of lipogenesis. We then discuss the benefits and drawbacks of the main methods available to measure fatty acid synthesis and adult fat accumulation. Most importantly, gravimetric/colorimetric and isotope tracking methods give complementary information, provided that they are applied with appropriate controls and interpreted correctly. We also compiled a comprehensive list of fat accumulation studies performed during the last 25 years. We present avenues for future research that combine chemistry, ecology, and evolution into an integrative approach, which we think is needed to understand the dynamics of fat accumulation in parasitoids.

The Drosophila-parasitizing wasp Leptopilina heterotoma: A comprehensive model system in ecology and evolution.

The parasitoid Leptopilina heterotoma has been used as a model system for more than 70 years, contributing greatly to diverse research areas in ecology and evolution. Here, we synthesized the large body of work on L. heterotoma with the aim to identify new research avenues that could be of interest also for researchers studying other parasitoids and insects. We start our review with a description of typical L. heterotoma characteristics, as well as that of the higher taxonomic groups to which this species belongs. We then continue discussing host suitability and immunity, foraging behaviors, as well as fat accumulation and life histories. We subsequently shift our focus towards parasitoid-parasitoid interactions, including L. heterotoma coexistence within the larger guild of Drosophila parasitoids, chemical communication, as well as mating and population structuring. We conclude our review by highlighting the assets of L. heterotoma as a model system, including its intermediate life history syndromes, the ease of observing and collecting natural hosts and wasps, as well as recent genomic advances.

A Comparative Study of the Dynamics and Diversity of Bdellovibrio and Like Organisms in Lakes Annecy and Geneva.

Bdellovibrio and like organisms (BALOs) are obligate bacterial predators of other Gram-negative bacteria. Here, we used quantitative PCR (qPCR) and recently developed specific primers which target the 16S rRNA gene to explore the abundance and distribution of three families of BALO belonging to the Oligoflexia class (i.e., Bdellovibrionaceae, Peredibacteraceae and Bacteriovoracaceae) over one year in the epilimnion and hypolimnion of Lakes Annecy and Geneva. Peredibacteraceae was the dominant group at all sampling points except at the bottom of Lake Geneva, where Bdellovibrionaceae was found in higher number. In addition, the abundance of BALOs increased significantly during the warmer months. Using high-throughput sequencing (Illumina Miseq), hundreds of OTUs were identified for Bdellovibrionaceae and Peredibacteraceae. Phylogenetic analysis suggests that Bdellovibrionaceae are more diverse than Peredibacteraceae and that some OTUs belong to new species of Bdellovibrionaceae. We also found that dominant OTUs were present simultaneously in the two lakes, while some others were specific to each lake, suggesting an adaptive pattern. Finally, both abundance and diversity of BALOs were poorly associated with abiotic factors except temperature, suggesting the importance of studying biotic relationships, assumed to play a greater role than physico-chemical variables in BALOs' dynamics and distribution.

Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites.

BACKGROUND: Animal-associated microbial communities appear to be key factors in host physiology, ecology, evolution and its interactions with the surrounding environment. Teleost fish have received relatively little attention in the study of surface-associated microbiota. Besides the important role of microbiota in homeostasis and infection prevention, a few recent studies have shown that fish mucus microbiota may interact with and attract some specific parasitic species. However, our understanding of external microbial assemblages, in particular regarding the factors that determine their composition and potential interactions with parasites, is still limited. This is the objective of the present study that focuses on a well-known fish-parasite interaction, involving the Sparidae (Teleostei), and their specific monogenean ectoparasites of the Lamellodiscus genus. We characterized the skin and gill mucus bacterial communities using a 16S rRNA amplicon sequencing, tested how fish ecological traits and host evolutionary history are related to external microbiota, and assessed if some microbial taxa are related to some Lamellodiscus species. RESULTS: Our results revealed significant differences between skin and gill microbiota in terms of diversity and structure, and that sparids establish and maintain tissue and species-specific bacterial communities despite continuous exposure to water. No phylosymbiosis pattern was detected for either gill or skin microbiota, suggesting that other host-related and environmental factors are a better regulator of host-microbiota interactions. Diversity and structure of external microbiota were explained by host traits: host species, diet and body part. Numerous correlations between the abundance of given bacterial genera and the abundance of given Lamellodiscus species have been found in gill mucus, including species-specific associations. We also found that the external microbiota of the only unparasitized sparid species in this study, Boops boops, harbored significantly more Fusobacteria and three genera, Shewenella, Cetobacterium and Vibrio, compared to the other sparid species, suggesting their potential involvement in preventing monogenean infection. CONCLUSIONS: This study is the first to explore the diversity and structure of skin and gill microbiota from a wild fish family and present novel evidence on the links between gill microbiota and monogenean species in diversity and abundance, paving the way for further studies on understanding host-microbiota-parasite interactions.

Host specificity of monogenean ectoparasites on fish skin and gills assessed by a metabarcoding approach.

Monogeneans are highly diverse fish ectoparasites with a direct life cycle, widely distributed, and are known to generally display strict host specificity. Factors related to the hosts and the parasite have been suggested to explain this high specificity. Monogeneans have also been observed to colonise fish species not in their natural host range under experimental conditions. We developed a specific metabarcoding protocol and applied it on the Sparidae-Lamellodiscus host-parasite system, to assess parasite diversity on skin and gills of several sparid host species. We first demonstrated that the use of a metabarcoding approach provided a better understanding of the diversity of monogeneans associated with teleost skin and gills than traditional approaches based on morphological identification. We identified a high diversity of both expected and unexpected (never observed on this host species) Lamellodiscus spp. on each host species and on skin and gills. No significant difference in parasite diversity was found between skin and gills. These results suggest that the establishment of the observed host specificity in monogeneans relies on multiple levels of regulation, involving the survival capacity of the larvae and host recognition mechanisms.

High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation?

The epicontinental fauna of the Iberian Peninsula is strongly influenced by its geographical history. As the possibilities for dispersion of organisms into and from this region were (and still are) limited, the local fauna consists almost exclusively of endemic species. Almost all Iberian freshwater fishes of the families Leuciscidae and Cyprinidae are endemic and on-going research on these taxa continually uncovers new species. Nevertheless, information on their host-specific parasites remains scarce. In this study, we investigate the diversity and phylogenetic relationships in monogeneans of the genus Dactylogyrus (gill ectoparasites specific to cyprinoid fish) in the Iberian Peninsula. Twenty-two species were collected and identified from 19 host species belonging to Cyprinidae and Leuciscidae. A high degree of endemism was observed, with 21 Dactylogyrus species reported from Iberia only and a single species, D. borealis, also reported from other European regions. Phylogenetic analysis split the endemic Iberian Dactylogyrus into two well-supported clades, the first encompassing Dactylogyrus parasitizing endemic Luciobarbus spp. only, and the second including all Dactylogyrus species of endemic leuciscids and four species of endemic cyprinids. Species delimitation analysis suggests a remarkable diversity and existence of a multitude of cryptic Dactylogyrus species parasitizing endemic leuciscids (Squalius spp. and representatives of Chondrostoma s.l.). These results suggest a rapid adaptive radiation of Dactylogyrus in this geographically isolated region, closely associated with their cyprinoid hosts. Moreover, phylogenetic analysis supports that Dactylogyrus parasites colonized the Iberian Peninsula through multiple dispersion events.

Low-diversity bacterial microbiota in Southern Ocean representatives of lanternfish genera Electrona, Protomyctophum and Gymnoscopelus (family Myctophidae).

Myctophids are among the most abundant mesopelagic teleost fishes worldwide. They are dominant in the Southern Ocean, an extreme environment where they are important both as consumers of zooplankton as well as food items for larger predators. Various studies have investigated myctophids diet, but no data is yet available regarding their associated microbiota, despite that the significance of bacterial communities to fish health and adaptation is increasingly acknowledged. In order to document microbiota in key fish groups from the Southern Ocean, the bacterial communities associated with the gut, fin, gills and light organs of members of six species within the three myctophid genera Electrona, Protomyctophum and Gymnoscopelus were characterized using a 16S rRNA-based metabarcoding approach. Gut communities display limited diversity of mostly fish-specific lineages likely involved in food processing. Fin and skin communities display diversity levels and compositions resembling more those found in surrounding seawater. Community compositions are similar between genera Electrona and Protomyctophum, that differ from those found in Gymnoscopelus and in water. Low abundances of potentially light-emitting bacteria in light organs support the hypothesis of host production of light. This first description of myctophid-associated microbiota, and among the first on fish from the Southern Ocean, emphasizes the need to extend microbiome research beyond economically-important species, and start addressing ecologically-relevant species.

Characterization of ecto- and endoparasite communities of wild Mediterranean teleosts by a metabarcoding approach.

Next-generation sequencing methods are increasingly used to identify eukaryotic, unicellular and multicellular symbiont communities within hosts. In this study, we analyzed the non-specific reads obtained during a metabarcoding survey of the bacterial communities associated to three different tissues collected from 13 wild Mediterranean teleost fish species. In total, 30 eukaryotic genera were identified as putative parasites of teleosts, associated to skin mucus, gills mucus and intestine: 2 ascomycetes, 4 arthropods, 2 cnidarians, 7 nematodes, 10 platyhelminthes, 4 apicomplexans, 1 ciliate as well as one order in dinoflagellates (Syndiniales). These results highlighted that (1) the metabarcoding approach was able to uncover a large spectrum of symbiotic organisms associated to the fish species studied, (2) symbionts not yet identified in several teleost species were putatively present, (3) the parasitic diversity differed markedly across host species and (4) in most cases, the distribution of known parasitic genera within tissues is in accordance with the literature. The current work illustrates the large insights that can be gained by making maximum use of data from a metabarcoding approach.