Shifts in marine invertebrate bacterial assemblages associated with tissue necrosis during a heat wave

Marine heat waves (MHWs) are periods of extremely high seawater temperature that affect marine ecosystems in several ways. Anthozoans (corals and gorgonians) and Porifera (sponges) are usually among the taxa most affected by MHWs. Both are holobiont entities that form complex interactions with a wide range of microbes, which are an essential part of these organisms and play key roles in their health status. Here, we determine microbial community changes suffered in two corals (Cladocora caespitosa and Oculina patagonica), one gorgonian (Leptogorgia sarmentosa) and one sponge (Sarcotragus fasciculatus) during the 2015 MHW. The microbial communities were different among hosts and displayed shifts related to host health status, with a higher abundance in necrosed tissues of Ruegeria species or of potential pathogens like Vibrio. We also carry out a meta-analysis using 93 publicly accessible 16S rRNA gene libraries from O. patagonica, C. caespitosa and L. sarmentosa to establish a Mediterranean core microbiome in these species. We have identified one Ruegeria OTU that maintained a stable and consistent association with these species, which was also related to tissue necrosis in their hosts. Therefore, Ruegeria sp. could play an important and still underexplored role in the health status of its hosts.This work has been carried out within the CIESM project “Tropical Signals” and it was funded by the European Union’s framework program Horizon 2020 (LEIT-BIO-2015-685474, Metafluidics, to JA)

Sipuncula inhabiting the coral Oculina patagonica in the western Mediterranean Sea

Background: We analyzed the sipunculan fauna inhabiting the scleractinian coral Oculina patagonica in the Marine Reserve of Tabarca Island (western Mediterranean). Results: Five sipunculan species were collected from 2011 to 2014: Phascolosoma stephensoni, P. granulatum, P. cf. agassizii, Aspidosiphon misakiensis, and Golfingia vulgaris. All five species were reported for the first time inhabiting O. patagonica; with P. cf. agassizii being a new record for the Iberian Peninsula. The average abundance of sipunculans inhabiting the coral was 468.75 ± 158.04 ind m−2, representing the second most abundant taxonomic group, in biomass, after Mollusca. Conclusions: Sipunculan diversity was low comparing with tropical reefs, but species abundances were higher than in soft-bottom nearby areas and community structure appears to be more homogeneous. There may be a considerable contribution to the erosion of the coral skeleton by sipunculans

Exploring changes in bacterial communities to assess the influence of fish farming on marine sediments

Changes in bacterial assemblages along an environmental gradient determined by the distance to aquaculture installations were analysed, using denaturing gradient gel electrophoresis to assess the influence of fish farming on marine sediments. Our findings show that changes in the structure of the bacterial community are a useful indicator for determining the environmental impact of aquaculture farms, due to the rapid response to changes in nutrient load, and could be an alternative strategy for monitoring programmes. Delta and Epsilonproteobacteria linked to the sulphur cycle were detected in the sediments beneath the cages. Since these groups were not found in the sediments at control stations, they serve as indicators for assessing the impact of the organic load from fish farming on marine sediments.This study forms part of the ‘Selección de indicadores, determinación de valores de referencia, diseño de programas y protocolos de métodos y medidas para estudios ambientales en acuicultura marina’ project funded by the ‘Spanish National Plans of Aquaculture’ (JACUMAR). The research was supported by Spanish Ministry of Economy and Competitiveness project CLG2015_66686-C3-3 (JA), which was also supported by financing from the European Regional Development Fund (FEDER). ERP thanks the Generalitat Valenciana for a postdoctoral grant (APOSTD-2016-091)

Biogeographic Differences in the Microbiome and Pathobiome of the Coral Cladocora caespitosa in the Western Mediterranean Sea.

The endemic Mediterranean zooxanthellate scleractinian reef-builder Cladocora caespitosa is among the organisms most affected by warming-related mass mortality events in the Mediterranean Sea. Corals are known to contain a diverse microbiota that plays a key role in their physiology and health. Here we report the first study that examines the microbiome and pathobiome associated with C. caespitosa in three different Mediterranean locations (i.e., Genova, Columbretes Islands, and Tabarca Island). The microbial communities associated with this species showed biogeographical differences, but shared a common core microbiome that probably plays a key role in the coral holobiont. The putatively pathogenic microbial assemblage (i.e., pathobiome) of C. caespitosa also seemed to depend on geographic location and the human footprint. In locations near the coast and with higher human influence, the pathobiome was entirely constituted by Vibrio species, including the well-known coral pathogens Vibrio coralliilyticus and V. mediterranei. However, in the Columbretes Islands, located off the coast and the most pristine of the analyzed locations, no changes among microbial communities associated to healthy and necrosed samples were detected. Hence, our results provide new insights into the microbiome of the temperate corals and its role in coral health status, highlighting its dependence on the local environmental conditions and the human footprint

Virulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens

The increase in prevalence and severity of coral disease outbreaks produced by Vibrio pathogens, and related to global warming, has seriously impacted reef-building corals throughout the oceans. The coral Oculina patagonica has been used as a model system to study coral bleaching produced by Vibrio infection. Previous data demonstrated that when two coral pathogens (Vibrio coralliilyticus and Vibrio mediterranei) simultaneously infected the coral O. patagonica, their pathogenicity was greater than when each bacterium was infected separately. Here, to understand the mechanisms underlying this synergistic effect, transcriptomic analyses of monocultures and cocultures as well as experimental infection experiments were performed. Our results revealed that the interaction between the two vibrios under culture conditions overexpressed virulence factor genes (e.g., those encoding siderophores, the type VI secretion system, and toxins, among others). Moreover, under these conditions, vibrios were also more likely to form biofilms or become motile through induction of lateral flagella. All these changes that occur as a physiological response to the presence of a competing species could favor the colonization of the host when they are present in a mixed population. Additionally, during coral experimental infections, we showed that exposure of corals to molecules released during V. coralliilyticus and V. mediterranei coculture induced changes in the coral microbiome that favored damage to coral tissue and increased the production of lyso-platelet activating factor. Therefore, we propose that competition sensing, defined as the physiological response to detection of harm or to the presence of a competing Vibrio species, enhances the ability of Vibrio coral pathogens to invade their host and cause tissue necrosis.This research was supported in part by the EU-H2020 MetaFluidics project with grant agreement number 685474 (to J.A.) and NSF-PIRE grant number OISE1243541 (to F.R.). E.R.-P. was funded by the postdoctoral program Vali+d (GVA) (grant number APOSTD-2016-091). A.M.C.-R. and P.C.D. were supported by the National Sciences Foundation grant IOS-1656481

Effects of the 2015 heat wave on benthic invertebrates in the Tabarca Marine Protected Area (southeast Spain)

In the late summer of 2015, extensive mortality of scleratinian corals, gorgonians, and sponges was observed in the Marine Protected Area of Tabarca (southeast Spain). Quantitative data indicated that at 25 m depth the sea fan Eunicella singularis was the most affected species (50% of colonies affected by partial mortality); while in shallow waters more than 40% of the endemic scleractinian coral Cladocora caespitosa population showed tissue lesions that affected more than 10% of their surfaces. Other affected species were the scleractinian corals Oculina patagonica and Phyllangia mouchezii, the sea fan Leptogorgia sarmentosa and the sponge Sarcotragus fasciculatus. This mortality event coincided with an abnormal rise in seawater temperature in this region. Microbiological analysis showed a higher abundance of culturable Vibrio species in invertebrates exhibiting tissue lesions, which indicated that these opportunistic pathogens could be a key factor in the process

Factors structuring microbial communities in highly impacted coastal marine sediments (Mar Menor lagoon, SE Spain)

Coastal marine lagoons are environments highly vulnerable to anthropogenic pressures such as agriculture nutrient loading or runoff from metalliferous mining. Sediment microorganisms, which are key components in the biogeochemical cycles, can help attenuate these impacts by accumulating nutrients and pollutants. The Mar Menor, located in the southeast of Spain, is an example of a coastal lagoon strongly altered by anthropic pressures, but the microbial community inhabiting its sediments remains unknown. Here, we describe the sediment prokaryotic communities along a wide range of environmental conditions in the lagoon, revealing that microbial communities were highly heterogeneous among stations, although a core microbiome was detected. The microbiota was dominated by Delta- and Gammaproteobacteria and members of the Bacteroidia class. Additionally, several uncultured groups such as Asgardarchaeota were detected in relatively high proportions. Sediment texture, the presence of Caulerpa or Cymodocea, depth, and geographic location were among the most important factors structuring microbial assemblages. Furthermore, microbial communities in the stations with the highest concentrations of potentially toxic elements (Fe, Pb, As, Zn, and Cd) were less stable than those in the non-contaminated stations. This finding suggests that bacteria colonizing heavily contaminated stations are specialists sensitive to change.The study of the microbial communities has been carried out within the project “Metafluidics” and it was funded by the European Union’s framework program Horizon 2020 (LEIT-BIO-2015-685474 to JA). Samplings were supported by the projects MEMM (financed by the Spanish Institute of Oceanography), 19-ESMARES2-ANG (financed by the Spanish Ministry of Ecological Transition and Demographic Challenge), and BIOFOM (Ref. TEC0004869 financed by the Regional Government of Murcia). M-DB and JB-E were supported by a contract within the Program Personal Técnico de Apoyo funded by the Ministerio de Economía y Competitividad. BA-R was also supported by the ACIF fellow of the Generalitat Valenciana government

Factors structuring microbial communities in highly impacted coastal marine sediments (Mar Menor lagoon, SE Spain)

Coastal marine lagoons are environments highly vulnerable to anthropogenic pressures such as agriculture nutrient loading or runoff from metalliferous mining. Sediment microorganisms, which are key components in the biogeochemical cycles, can help attenuate these impacts by accumulating nutrients and pollutants. The Mar Menor, located in the southeast of Spain, is an example of a coastal lagoon strongly altered by anthropic pressures, but the microbial community inhabiting its sediments remains unknown. Here, we describe the sediment prokaryotic communities along a wide range of environmental conditions in the lagoon, revealing that microbial communities were highly heterogeneous among stations, although a core microbiome was detected. The microbiota was dominated by Delta- and Gammaproteobacteria and members of the Bacteroidia class. Additionally, several uncultured groups such as Asgardarchaeota were detected in relatively high proportions. Sediment texture, the presence of Caulerpa or Cymodocea, depth, and geographic location were among the most important factors structuring microbial assemblages. Furthermore, microbial communities in the stations with the highest concentrations of potentially toxic elements (Fe, Pb, As, Zn, and Cd) were less stable than those in the non-contaminated stations. This finding suggests that bacteria colonizing heavily contaminated stations are specialists sensitive to change

New Mediterranean Biodiversity Records (July 2016)

This contribution forms part of a series of collective articles published regularly in Mediterranean Marine Science that report on new biodiversity records from the Mediterranean basin. The current article presents 51 geographically distinct records for 21 taxa belonging to 6 Phyla, extending from the western Mediterranean to the Levantine. The new records, per country, are as follows: Spain: the cryptogenic calcareous sponge Paraleucilla magna is reported from a new location in the Alicante region. Algeria: the rare Atlanto-Mediterranean bivalve Cardium indicum is reported from Annaba. Tunisia: new distribution records for the Indo-Pacific lionfish Pterois miles from Zembra Island and Cape Bon. Italy: the ark clam Anadara transversa is reported from mussel cultures in the Gulf of Naples, while the amphipod Caprella scaura and the isopods Paracerceis sculpta and Paranthura japonica are reported as associated to the –also allochthonous–bryozoan Amathia verticillata in the Adriatic Sea; in the latter region, the cosmopolitan Atlantic tripletail Lobotes surinamensisis also reported, a rare finding for the Mediterranean. Slovenia: a new record of the non-indigenous nudibranch Polycera hedgpethi in the Adriatic. Greece: several new reports of the introduced scleractinian Oculina patagonica, the fangtooth moray Enchelycore anatina, the blunthead puffer Sphoeroides pachygaster (all Atlantic), and the lionfish Pterois miles (Indo-Pacific) suggest their ongoing establishment in the Aegean Sea; the deepest bathymetric record of the invasive alga Caulerpa cylindracea in the Mediterranean Sea is also registered in the Kyklades, at depths exceeding 70 m. Turkey: new distribution records for two non indigenous crustaceans, the blue crab Callinectes sapidus (Atlantic origin) and the moon crab Matuta victor (Indo-Pacific origin) from the Bay of Izmir and Antalya, respectively; in the latter region, the Red Sea goatfish Parupeneus forsskali, is also reported. Lebanon: an array of records of 5 alien and one native Mediterranean species is reported by citizen-scientists; the Pacific jellyfish Phyllorhiza punctata and the Indo-Pacific teleosteans Tylerius spinosissimus, Ostracion cubicus, and Lutjanus argentimaculatus are reported from the Lebanese coast, the latter notably being the second record for the species in the Mediterranean Sea since 1977; the native sand snake-eel Ophisurus serpens, rare in the eastern Mediterranean, is reported for the first time from Lebanon, this being its easternmost distribution range; finally, a substantial number of sightings of the lionfish Pterois miles further confirm the current establishment of this lessepsian species in the Levantine

Consensus Guidelines for Advancing Coral Holobiont Genome and Specimen Voucher Deposition

Coral research is being ushered into the genomic era. To fully capitalize on the potential discoveries from this genomic revolution, the rapidly increasing number of high-quality genomes requires effective pairing with rigorous taxonomic characterizations of specimens and the contextualization of their ecological relevance. However, to date there is no formal framework that genomicists, taxonomists, and coral scientists can collectively use to systematically acquire and link these data. Spurred by the recently announced “Coral symbiosis sensitivity to environmental change hub” under the “Aquatic Symbiosis Genomics Project” - a collaboration between the Wellcome Sanger Institute and the Gordon and Betty Moore Foundation to generate gold-standard genome sequences for coral animal hosts and their associated Symbiodiniaceae microalgae (among the sequencing of many other symbiotic aquatic species) - we outline consensus guidelines to reconcile different types of data. The metaorganism nature of the coral holobiont provides a particular challenge in this context and is a key factor to consider for developing a framework to consolidate genomic, taxonomic, and ecological (meta)data. Ideally, genomic data should be accompanied by taxonomic references, i.e., skeletal vouchers as formal morphological references for corals and strain specimens in the case of microalgal and bacterial symbionts (cultured isolates). However, exhaustive taxonomic characterization of all coral holobiont member species is currently not feasible simply because we do not have a comprehensive understanding of all the organisms that constitute the coral holobiont. Nevertheless, guidelines on minimal, recommended, and ideal-case descriptions for the major coral holobiont constituents (coral animal, Symbiodiniaceae microalgae, and prokaryotes) will undoubtedly help in future referencing and will facilitate comparative studies. We hope that the guidelines outlined here, which we will adhere to as part of the Aquatic Symbiosis Genomics Project sub-hub focused on coral symbioses, will be useful to a broader community and their implementation will facilitate cross- and meta-data comparisons and analyses.CV acknowledges funding from the German Research Foundation (DFG), grants 433042944 and 458901010. Open Access publication fees are covered by an institutional agreement of the University of Konstanz