Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiency

Ocean acidification significantly affects marine organisms in several ways, with complex interactions. Seaweeds might benefit from rising CO2 through increased photosynthesis and carbon acquisition, with subsequent higher growth rates. However, changes in seaweed chemistry due to increased CO2 may change the nutritional quality of tissue for grazers. In addition, organisms live in close association with a diverse microbiota, which can also be influenced by environmental changes, with feedback effects. As gut microbiomes are often linked to diet, changes in seaweed characteristics and associated microbiome can affect the gut microbiome of the grazer, with possible fitness consequences. In this study, we experimentally investigated the effects of acidification on the microbiome of the invasive brown seaweed Sargassum muticum and a native isopod consumer Synisoma nadejda. Both were exposed to ambient CO2 conditions (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three weeks. Microbiome diversity and composition were determined using high-throughput sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result of acidification, the seaweed-associated bacterial community would change, leading to further changes in the gut microbiome of grazers. However, no significant effects of elevated CO2 on the overall bacterial community structure and composition were revealed in the seaweed. In contrast, significant changes were observed in the bacterial community of the grazer gut. Although the bacterial community of S. muticum as whole did not change, Oceanospirillales and Vibrionales (mainly Pseudoalteromonas) significantly increased their abundance in acidified conditions. The former, which uses organic matter compounds as its main source, may have opportunistically taken advantage of the possible increase of the C/N ratio in the seaweed under acidified conditions. Pseudoalteromonas, commonly associated to diseased seaweeds, suggesting that acidification may facilitate opportunistic/pathogenic bacteria. In the gut of S. nadejda, the bacterial genus Planctomycetia increased abundance under elevated CO2. This shift might be associated to changes in food (S. muticum) quality under acidification. Planctomycetia are slow-acting decomposers of algal polymers that could be providing the isopod with an elevated algal digestion and availability of inorganic compounds to compensate the shifted C/N ratio under acidification in their food. In conclusion, our results indicate that even after only three weeks of acidified conditions, bacterial communities associated to ungrazed seaweed and to an isopod grazer show specific, differential shifts in associated bacterial community. These have potential consequences for seaweed health (as shown in corals) and isopod food digestion. The observed changes in the gut microbiome of the grazer seem to reflect changes in the seaweed chemistry rather than its microbial composition.Erasmus Mundus Doctoral Programme MARES on Marine Ecosystem Health Conservation [MARES_13_08]; FCT (Foundation for Science and Technology, Portugal) [SFRH/BPD/63703/2009, SFRH/BPD/107878/2015, SFRH/BPD/116774/2016]; EU SEAS-ERA project INVASIVES [SEAS-ERA/0001/2012]; [CCMAR/Multi/04326/2013

A Modified View on Octocorals: Heteroxenia fuscescens Nematocysts Are Diverse, Featuring Both an Ancestral and a Novel Type

Cnidarians are characterized by the presence of stinging cells containing nematocysts, a sophisticated injection system targeted mainly at prey-capture and defense. In the anthozoan subclass Octocorallia nematocytes have been considered to exist only in low numbers, to be small, and all of the ancestral atrichous-isorhiza type. This study, in contrast, revealed numerous nematocytes in the octocoral Heteroxenia fuscescens. The study demonstrates the applicability of cresyl-violet dye for differential staining and stimulating discharge of the nematocysts. In addition to the atrichous isorhiza-type of nematocysts, a novel type of macrobasic-mastigophore nematocysts was found, featuring a shaft, uniquely comprised of three loops and densely packed arrow-like spines. In contrast to the view that octocorals possess a single type of nematocyst, Heteroxenia fuscescens features two distinct types, indicating for the first time the diversification and complexity of nematocysts for Octocorallia

Shared Skeletal Support in a Coral-Hydroid Symbiosis

Hydroids form symbiotic relationships with a range of invertebrate hosts. Where they live with colonial invertebrates such as corals or bryozoans the hydroids may benefit from the physical support and protection of their host's hard exoskeleton, but how they interact with them is unknown. Electron microscopy was used to investigate the physical interactions between the colonial hydroid Zanclea margaritae and its reef-building coral host Acropora muricata. The hydroid tissues extend below the coral tissue surface sitting in direct contact with the host's skeleton. Although this arrangement provides the hydroid with protective support, it also presents problems of potential interference with the coral's growth processes and exposes the hydroid to overgrowth and smothering. Desmocytes located within the epidermal layer of the hydroid's perisarc-free hydrorhizae fasten it to the coral skeleton. The large apical surface area of the desmocyte and high bifurcation of the distal end within the mesoglea, as well as the clustering of desmocytes suggests that a very strong attachment between the hydroid and the coral skeleton. This is the first study to provide a detailed description of how symbiotic hydroids attach to their host's skeleton, utilising it for physical support. Results suggest that the loss of perisarc, a characteristic commonly associated with symbiosis, allows the hydroid to utilise desmocytes for attachment. The use of these anchoring structures provides a dynamic method of attachment, facilitating detachment from the coral skeleton during extension, thereby avoiding overgrowth and smothering enabling the hydroid to remain within the host colony for prolonged periods of time

Bacterial Symbiosis Maintenance in the Asexually Reproducing and Regenerating Flatworm Paracatenula galateia

Bacteriocytes set the stage for some of the most intimate interactions between animal and bacterial cells. In all bacteriocyte possessing systems studied so far, de novo formation of bacteriocytes occurs only once in the host development, at the time of symbiosis establishment. Here, we present the free-living symbiotic flatworm Paracatenula galateia and its intracellular, sulfur-oxidizing bacteria as a system with previously undescribed strategies of bacteriocyte formation and bacterial symbiont transmission. Using thymidine analogue S-phase labeling and immunohistochemistry, we show that all somatic cells in adult worms – including bacteriocytes – originate exclusively from aposymbiotic stem cells (neoblasts). The continued bacteriocyte formation from aposymbiotic stem cells in adult animals represents a previously undescribed strategy of symbiosis maintenance and makes P. galateia a unique system to study bacteriocyte differentiation and development. We also provide morphological and immunohistochemical evidence that P. galateia reproduces by asexual fragmentation and regeneration (paratomy) and, thereby, vertically transmits numerous symbiont-containing bacteriocytes to its asexual progeny. Our data support the earlier reported hypothesis that the symbiont population is subjected to reduced bottleneck effects. This would justify both the codiversification between Paracatenula hosts and their Candidatus Riegeria symbionts, and the slow evolutionary rates observed for several symbiont genes

From Parent to Gamete: Vertical Transmission of Symbiodinium (Dinophyceae) ITS2 Sequence Assemblages in the Reef Building Coral Montipora capitata

Parental effects are ubiquitous in nature and in many organisms play a particularly critical role in the transfer of symbionts across generations; however, their influence and relative importance in the marine environment has rarely been considered. Coral reefs are biologically diverse and productive marine ecosystems, whose success is framed by symbiosis between reef-building corals and unicellular dinoflagellates in the genus Symbiodinium. Many corals produce aposymbiotic larvae that are infected by Symbiodinium from the environment (horizontal transmission), which allows for the acquisition of new endosymbionts (different from their parents) each generation. In the remaining species, Symbiodinium are transmitted directly from parent to offspring via eggs (vertical transmission), a mechanism that perpetuates the relationship between some or all of the Symbiodinium diversity found in the parent through multiple generations. Here we examine vertical transmission in the Hawaiian coral Montipora capitata by comparing the Symbiodinium ITS2 sequence assemblages in parent colonies and the eggs they produce. Parental effects on sequence assemblages in eggs are explored in the context of the coral genotype, colony morphology, and the environment of parent colonies. Our results indicate that ITS2 sequence assemblages in eggs are generally similar to their parents, and patterns in parental assemblages are different, and reflect environmental conditions, but not colony morphology or coral genotype. We conclude that eggs released by parent colonies during mass spawning events are seeded with different ITS2 sequence assemblages, which encompass phylogenetic variability that may have profound implications for the development, settlement and survival of coral offspring

Cyanotoxins are not implicated in the etiology of coral black band disease outbreaks on Pelorus Island, Great Barrier Reef

Cyanobacterial toxins (i.e. microcystins) produced within the microbial mat of coral black band disease (BBD) have been implicated in disease pathogenicity. This study investigated the presence of toxins within BBD lesions and other cyanobacterial patch (CP) lesions, which, in some instances (∼19%), facilitated the onset of BBD, from an outbreak site at Pelorus Island on the inshore, central Great Barrier Reef (GBR). Cyanobacterial species that dominated the biomass of CP and BBD lesions were cultivated and identified, based on morphology and 16S rRNA gene sequences, as Blennothrix- and Oscillatoria-affiliated species, respectively, and identical to cyanobacterial sequences retrieved from previous molecular studies from this site. The presence of the cyanotoxins microcystin, cylindrospermopsin, saxitoxin, nodularin and anatoxin and their respective gene operons in field samples of CP and BBD lesions and their respective culture isolations was tested using genetic (PCR-based screenings), chemical (HPLC-UV, FTICR-MS and LC/MSn) and biochemical (PP2A) methods. Cyanotoxins and cyanotoxin synthetase genes were not detected in any of the samples. Cyanobacterial species dominant within CP and BBD lesions were phylogenetically distinct from species previously shown to produce cyanotoxins and isolated from BBD lesions. The results from this study demonstrate that cyanobacterial toxins appear to play no role in the pathogenicity of CP and BBD at this site on the GBR

Association of Waminoa sp. (Acoela) with corals in the Wakatobi Marine Park, South-East Sulawesi, Indonesia

This is the first quantitative study on the prevalence of epizoic Waminoa sp. acoel worms and their association with corals in the Wakatobi Marine National Park (WMNP), South-East Sulawesi, Indonesia. Three replicate transects were laid on the reef crest, flat and slope at six sites in 2006 and eight sites in 2007. Four of the sites were common in both years. In total 69 transects were surveyed in 2006, and 87 transects in 2007. A total of 4.8% of all observed hard corals were associated with acoel worms in 2006 and 2.6% of hard and soft corals in 2007. Acoels were present on 16 and 21 of the coral taxa studied in 2006 and 2007 respectively. The worms were strongly associated with the azooxanthellate coral Tubastrea spp. and were rare or absent on the most abundant coral genera Montipora and Porites. The mean number of corals having acoels was highest on reef slopes, whereas acoels were virtually absent on reef flats. Corals that had a high and a medium cover of worms were more common in 2007 than in 2006. No significant trend in the adaptation of the zooxanthellae of Waminoa sp. to different depths at different sites was revealed. The impact of the worm on the coral is unknown, but high numbers may have a shading effect and a negative impact on the coral's photophysiology. This acoel merits more study of its life cycle, its photophysiology, and its impact on its host corals. © 2009 Springer-Verlag