Transcriptomic Evidence That Longevity of Acquired Plastids in the Photosynthetic Slugs Elysia timida and Plakobranchus ocellatus Does Not Entail Lateral Transfer of Algal Nuclear Genes

Sacoglossan sea slugs are unique in the animal kingdom in that they sequester and maintain active plastids that they acquire from the siphonaceous algae upon which they feed, making the animals photosynthetic. Although most sacoglossan species digest their freshly ingested plastids within hours, four species from the family Plakobranchidae retain their stolen plastids (kleptoplasts) in a photosynthetically active state on timescales of weeks to months. The molecular basis of plastid maintenance within the cytosol of digestive gland cells in these photosynthetic metazoans is yet unknown but is widely thought to involve gene transfer from the algal food source to the slugs based upon previous investigations of single genes. Indeed, normal plastid development requires hundreds of nuclear-encoded proteins, with protein turnover in photosystem II in particular known to be rapid under various conditions. Moreover, only algal plastids, not the algal nuclei, are sequestered by the animals during feeding. If algal nuclear genes are transferred to the animal either during feeding or in the germ line, and if they are expressed, then they should be readily detectable with deep-sequencing methods. We have sequenced expressed mRNAs from actively photosynthesizing, starved individuals of two photosynthetic sea slug species, Plakobranchus ocellatus Van Hasselt, 1824 and Elysia timida Risso, 1818. We find that nuclear-encoded, algal-derived genes specific to photosynthetic function are expressed neither in P. ocellatus nor in E. timida. Despite their dramatic plastid longevity, these photosynthetic sacoglossan slugs do not express genes acquired from algal nuclei in order to maintain plastid function

Reexamination of the species assignment of Diacavolinia pteropods using DNA barcoding

© The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS ONE 8 (2013): e53889, doi:10.1371/journal.pone.0053889.Thecosome pteropods (Mollusca, Gastropoda) are an ecologically important, diverse, and ubiquitous group of holoplanktonic animals that are the focus of intense research interest due to their external aragonite shell and vulnerability to ocean acidification. Characterizing the response of these animals to low pH and other environmental stressors has been hampered by continued uncertainty in their taxonomic identification. An example of this confusion in species assignment is found in the genus Diacavolinia. All members of this genus were originally indentified as a single species, Cavolinia longirostris, but over the past fifty years the taxonomy has been revisited multiple times; currently the genus comprises 22 different species. This study examines five species of Diacavolinia, including four sampled in the Northeast Atlantic (78 individuals) and one from the Eastern tropical North Pacific (15 individuals). Diacavolina were identified to species based on morphological characteristics according to the current taxonomy, photographed, and then used to determine the sequence of the “DNA barcoding” region of the cytochrome c oxidase subunit I (COI). Specimens from the Atlantic, despite distinct differences in shell morphology, showed polyphyly and a genetic divergence of <3% (K2P distance) whereas the Pacific and Atlantic samples were more distant (~19%). Comparisons of Diacavolinia spp. with other Cavolinia spp. reveal larger distances (~24%). These results indicate that specimens from the Atlantic comprise a single monophyletic species and suggest possible species-level divergence between Atlantic and Pacific populations. The findings support the maintenance of Diacavolinia as a separate genus, yet emphasize the inadequacy of our current taxonomic understanding of pteropods. They highlight the need for accurate species identifications to support estimates of biodiversity, range extent and natural exposure of these planktonic calcifiers to environmental variability; furthermore, the apparent variation of the pteropods shell may have implications for our understanding of the species’ sensitivity to ocean acidification.This material is based upon work supported by the National Science Foundation under Grant Number OCE-0928801. AEM was funded through the WHOI Postdoctoral Scholarship. Support to LBB was provided by the College of Liberal Arts & Sciences, University of Connecticut; and by the Census of Marine Life/Alfred P. Sloan Foundation

Alpine Crossroads or Origin of Genetic Diversity? Comparative Phylogeography of Two Sympatric Microgastropod Species

The Alpine Region, constituting the Alps and the Dinaric Alps, has played a major role in the formation of current patterns of biodiversity either as a contact zone of postglacial expanding lineages or as the origin of genetic diversity. In our study, we tested these hypotheses for two widespread, sympatric microgastropod taxa – Carychium minimum O.F. Müller, 1774 and Carychium tridentatum (Risso, 1826) (Gastropoda, Eupulmonata, Carychiidae) – by using COI sequence data and species potential distribution models analyzed in a statistical phylogeographical framework. Additionally, we examined disjunct transatlantic populations of those taxa from the Azores and North America. In general, both Carychium taxa demonstrate a genetic structure composed of several differentiated haplotype lineages most likely resulting from allopatric diversification in isolated refugial areas during the Pleistocene glacial periods. However, the genetic structure of Carychium minimum is more pronounced, which can be attributed to ecological constraints relating to habitat proximity to permanent bodies of water. For most of the Carychium lineages, the broader Alpine Region was identified as the likely origin of genetic diversity. Several lineages are endemic to the broader Alpine Region whereas a single lineage per species underwent a postglacial expansion to (re)colonize previously unsuitable habitats, e.g. in Northern Europe. The source populations of those expanding lineages can be traced back to the Eastern and Western Alps. Consequently, we identify the Alpine Region as a significant ‘hot-spot’ for the formation of genetic diversity within European Carychium lineages. Passive dispersal via anthropogenic means best explains the presence of transatlantic European Carychium populations on the Azores and in North America. We conclude that passive (anthropogenic) transport could mislead the interpretation of observed phylogeographical patterns in general

Shelled pteropods in peril: Assessing vulnerability in a high CO2 ocean

The impact of anthropogenic ocean acidification (OA) on marine ecosystems is a vital concern facing marine scientists and managers of ocean resources. Euthecosomatous pteropods (holoplanktonic gastropods) represent an excellent sentinel for indicating exposure to anthropogenic OA because of the sensitivity of their aragonite shells to the OA conditions less favorable for calcification. However, an integration of observations, experiments and modelling efforts is needed to make accurate predictions of how these organisms will respond to future changes to their environment. Our understanding of the underlying organismal biology and life history is far from complete and must be improved if we are to comprehend fully the responses of these organisms to the multitude of stressors in their environment beyond OA. This review considers the present state of research and understanding of euthecosomatous pteropod biology and ecology of these organisms and considers promising new laboratory methods, advances in instrumentation (such as molecular, trace elements, stable isotopes, palaeobiology alongside autonomous sampling platforms, CT scanning and high-quality video recording) and novel field-based approaches (i.e. studies of upwelling and CO2 vent regions) that may allow us to improve our predictive capacity of their vulnerability and/or resilience. In addition to playing a critical ecological and biogeochemical role, pteropods can offer a significant value as an early-indicator of anthropogenic OA. This role as a sentinel species should be developed further to consolidate their potential use within marine environmental management policy making

Internal storage and production of symbiotic bacteria in the reproductive system of a tropical marine gastropod

The vestibular gland and egg masses of Dendrodoris nigra (Gastropoda: Opisthobranchia: Nudibranchia) were investigated histologically and ultra-structurally. A detailed description of the ultrastructure of the gland and the egg masses is given, and the presence of symbiotic bacteria in the vestibular gland and identical-appearing bacteria in the egg masses is reported for the first time. Hypotheses about the function of these bacteria in the reproductive system of D. nigra are presented

Histological investigations of Dendrodoris nigra (Gastropoda, Nudibranchia, Dendrodorididae).

The histology of the major organ systems (digestive, reproductive, nervous, circulatory, excretory and respiratory, as wdl as epidermis) of the nudibranch Dendrodoris nigra (Stimpson, 1855) arc described for the first time and the results are compared with those derived from other members of the Doridoidea. It is shown that some characters which have been used to differentiate the genus Dendrodoris Ehrenberg, 1831 from other doridoideans (i.e., retractability of gills, lack of hard structures in the anterior digestive system, presence of pericardial glands) are problematic when used for phylogenetic ,analysis. This is especially true when taking into consideration that little is known about details of these structures in the Doridoide, as a whole

Species diversity of opisthobranch molluscs on Lizard Island, Great Barrier Reef, Australia

During several visits from 1999 to 2004 to the Australian Museum Research Station on Lizard Island (LIRS) (Great Barrier Reef, Northern Section, Queensland, Australia) the authors collected 158 different opisthobranch species from the reefs and lagoon areas surrounding Lizard Island. The number of species found gives an estimate of the diversity of the opisthobranch fauna on the northern Great Barrier Reef. The manuscript also provides colour plates of most species found so far on Lizard Island that will facilitate species identification, data usage and further data collection

Skeletal organic matrices in molluscs: origin, evolution, diagenesis

8 pagesInternational audienceThe mollusc shell comprises a small amount of organic macromolecules, mostly proteins and polysaccharides, which, all together, constitute the skeletal organic matrix (SOM). In the recent years, the study of the SOM of about two dozens of mollusc species via transcriptomics and/or proteomics has led to the identification of hundreds of shell-associated proteins. This rapidly growing set of data allows several comparisons, shedding light on similarities and differences at the primary structure level and on some peculiar evolutionary mechanisms that may have affected SOM proteins. In addition, it constitutes a prerequisite for investigating the SOM repertoires of sub-fossils or fossil specimens, closely related to known extant species, in order to revisit diagenetic processes, i.e. how SOM proteins degrade during fossilization. These two aspects are briefly exemplified here: on the one hand, Aplysia californica, the sea hare, exhibits a vestigial internal shell that has kept a proteomic signature similar to that found in fully functional external shells. On the other hand, subfossil specimens of the giant clam Tridacna, collected in French Polynesia, precisely dated and analysed by proteomics for their SOM content, comprise several preserved proteins that can still be identified by their peptide signature, in spite of information losses likely due to diagenetic transformations