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- Acidification effects on biofouling communities: winners and losersPublication . Peck, Lloyd S.; Clark, Melody S.; Power, Deborah; Reis, Joao; Batista, Frederico; Harper, Elizabeth M.How ocean acidification affects marine life is a major concern for science and society. However, its impacts on encrusting biofouling communities, that are both the initial colonizers of hard substrata and of great economic importance, are almost unknown. We showed that community composition changed significantly, from 92% spirorbids, 3% ascidians and 4% sponges initially to 47% spirorbids, 23% ascidians and 29% sponges after 100days in acidified conditions (pH 7.7). In low pH, numbers of the spirorbid Neodexiospira pseudocorrugata were reduced x5 compared to controls. The two ascidians present behaved differently with Aplidium sp. decreasing x10 in pH 7.7, whereas Molgula sp. numbers were x4 higher in low pH than controls. Calcareous sponge (Leucosolenia sp.) numbers increased x2.5 in pH 7.7 over controls. The diatom and filamentous algal community was also more poorly developed in the low pH treatments compared to controls. Colonization of new surfaces likewise showed large decreases in spirorbid numbers, but numbers of sponges and Molgula sp. increased. Spirorbid losses appeared due to both recruitment failure and loss of existing tubes. Spirorbid tubes are comprised of a loose prismatic fabric of calcite crystals. Loss of tube materials appeared due to changes in the binding matrix and not crystal dissolution, as SEM analyses showed crystal surfaces were not pitted or dissolved in low pH conditions. Biofouling communities face dramatic future changes with reductions in groups with hard exposed exoskeletons and domination by soft-bodied ascidians and sponges.
- Asynchrony in settlement time between the closely related oysters Crassostrea angulata and C. gigas in Ria Formosa lagoon (Portugal)Publication . Batista, Frederico; G Fonseca, Vera; Ruano, Francisco; Boudry, PierreThe Portuguese oyster Crassostrea angulata and the Pacific oyster Crassostrea gigas are very closely related species originating from Asia that were introduced in Europe. The objectives of the present study were to determine if there is asynchrony in settlement time of C. angulata and C. gigas larvae in an area where both taxa coexist and if hybridization between the two species occurs throughout the breeding season. Oyster collectors were deployed every two weeks during one year in two different sites in Ria Formosa lagoon (Portugal) and the oysters that settled were genotyped with nuclear and mitochondrial markers. Settlement of Crassostrea sp. was observed from April to November 2004 (n = 694), with two distinct periods. In the first period (April), when 19% of the oysters settled, the haplotypes and alleles characteristic of C. gigas were mainly observed. In the following settlement period (July to November), the frequency of haplotypes and alleles of C. gigas decreased over time while those characteristics of C. angulata reached high frequencies by the end of the settlement period. Our results suggest that C. gigas was able to reproduce at lower temperatures than C. angulata in spring. However, the non-significant allelic disequilibrium observed during almost all settlement periods suggests that hybridization is widespread in time. The results obtained in the present study show that there are differences in the reproductive behavior between C. angulata and C. gigas that may limit gene flow between the two species.
- Evolution and diversity of alpha-carbonic anhydrases in the mantle of the Mediterranean mussel (Mytilus galloprovincialis)Publication . Cardoso, João CR; Ferreira, Vinicius; Zhang, Xushuai; Anjos, Liliana; Félix, Rute; Batista, Frederico; Power, DeborahThe α-carbonic anhydrases (α-CAs) are a large and ancient group of metazoan-specific enzymes. They generate bicarbonate from metabolic carbon dioxide and through calcium carbonate crystal formation play a key role in the regulation of mineralized structures. To better understand how α-CAs contribute to shell mineralization in the marine Mediterranean mussel (Mytilus galloprovincialis) we characterized them in the mantle. Phylogenetic analysis revealed that mollusc α-CA evolution was affected by lineage and species-specific events. Ten α-CAs were found in the Mediterranean mussel mantle and the most abundant form was named, MgNACR, as it grouped with oyster nacreins (NACR). Exposure of the Mediterranean mussel to reduced water salinity (18 vs 37 ppt), caused a significant reduction (p < 0.05) in mantle esterase activity and MgNACR transcript abundance (p < 0.05). Protonograms revealed multiple proteins in the mantle with α-CA hydratase activity and mapped to a protein with a similar size to that deduced for monomeric MgNACR. Our data indicate that MgNACR is a major α-CA enzyme in mantle and that by homology with oyster nacreins likely regulates mussel shell production. We propose that species-dependent α-CA evolution may contribute to explain the diversity of bivalve shell structures and their vulnerability to environmental changes.
- Insights on the association between somatic aneuploidy and ostreid herpesvirus 1 detection in the oysters Crassostrea gigas, C. angulata and their F1 hybridsPublication . Batista, Frederico; Lopez-Sanmartin, Monserrat; Boudry, Pierre; Navas, Jose I.; Ruano, Francisco; Renault, Tristan; Fonseca, Vera G.; Leitao, AlexandraCytogenetic abnormalities associated with viral infections, including from viruses of the Herpesvirales order, have been reported in vertebrate species. Ostreid herpesvirus 1 (OsHV-1) has been detected worldwide during mortality outbreaks of the Pacific oyster Crassostrea gigas. On the other hand, a high proportion of aneuploid cells in somatic tissues have been observed in C. gigas. In this study, we analysed the putative association between aneuploidy levels and the detection of OsHV-1 in gills of C. gigas, the Portuguese oyster C. angulata and their F1 hybrids cultured in Ria Formosa (Portugal). OsHV-1 was detected by PCR in 5.4% of the total of oysters analysed (n = 111) namely in 11.1%, 8.0% and 1.7% of C. gigas, C. angulata and F1 hybrid respectively. Sequencing analysis of a viral fragment amplified with the C2/C6 primer pair revealed a high similarity with the OsHV-1 reference type. Moreover, in situ hybridization confirmed the presence of OsHV-1 in gill tissue. Oysters where OsHV-1 was detected had a significantly higher mean percentage of aneuploid cells (25%) than the ones where the virus was not detected (18%). However, the overall low percentage of positive samples contrasted with the high mean percentage of aneuploidy observed, with 50% of the oysters analysed showing a percentage of aneuploid cells between 20% and 30%. We hypothesize that somatic aneuploidy may adversely affect oysters making them more prone to OsHV-1 infection, but the virus is unlikely to be the cause of somatic aneuploidy.
- Detection of Bonamia exitiosa in the European flat oyster Ostrea edulis in southern PortugalPublication . Batista, Frederico; Lopez-Sanmartin, M.; Grade, A.; Navas, J. I.; Ruano, F.Bonamiosis is a disease caused by protozoan parasites of the genus Bonamia (phylum Haplosporidia) that has been responsible for mass mortalities in different oyster species worldwide (for review see Bower 2011; Engelsma et al. 2014). Within the genus Bonamia, there are four known species, namely B. ostreae (Pichot et al. 1980), B. rougheyi (Farley, Wolff & Elston 1988), B. exitiosa (Hine, Cochennec-Laureau & Berthe 2001) and B. perspora (Carnegie et al. 2006). B. exitiosa was originally described in Ostrea chilensis in New Zealand (Hine et al. 2001), and since then, it has been observed in several other countries. In Europe, B. exitiosa was detected for the first time in 2007 in the Atlantic coast of Spain (Abollo et al. 2008).
- Elevated seawater temperatures decrease microbial diversity in the gut of mytilus coruscusPublication . Li, Yi-Feng; Yang, Na; Liang, Xiao; Yoshida, Asami; Osatomi, Kiyoshi; Power, Deborah; Batista, Frederico; Yang, Jin-LongThe gut microbial community is critical for the host immune system, and in recent years, it has been extensively studied in vertebrates using 'omic' technologies. In contrast, knowledge about how the interactions between water temperature and diet affect the gut microbiota of marine invertebrates that do not thermoregulate is much less studied. In the present study, the effect of elevated seawater temperature and diet (Isochrysis zhanjiangensis and Platymonas helgolandica var. tsingtaoensis) on the gut microbial community of the commercial mussel, Mytilus coruscus, was investigated. The 16S rRNA gene sequencing was used to characterize the microbial community in M. coruscus gut. The mortality of M. coruscus exposed to a high water temperature (31 degrees C) increased after 3 days and the diversity of the bacterial community in the gut of live M. coruscus was significantly reduced. For example, the abundance of Bacteroides (Bacteroidetes) and norank_Marinilabiaceae (Bacteroidetes) increased in the gut of M. coruscus fed I. zhanjiangensis. In M. coruscus fed P. helgolandica, the abundance of Arcobacter (Proteobacteria) and norank_Marinilabiaceae increased and the abundance of unclassified_Flavobacteriaceae (Bacteroidetes) decreased. The results obtained in the present study suggest that high temperatures favored the proliferation of opportunistic bacteria, including Bacteroides and Arcobacter, which may increase host susceptibility to disease. Microbial community composition of the gut in live M. coruscus was not impacted by the microalgal diet but it was modified in the group of mussels that died. The present study provides insight into the potential effects on the gut microbiome and mussel-bacteria interactions of rising seawater temperatures.
- Experimental infection of European flat oyster Ostrea edulis with ostreid herpesvirus 1 microvar (OsHV-1 mu var): Mortality, viral load and detection of viral transcripts by in situ hybridizationPublication . Sanmartin, Monserrat Lopez; Power, Deborah; de la Herran, Roberto; Navas, Jose I.; Batista, FredericoOstreid herpesvirus 1 (OsHV-1) infections have been reported in several bivalve species. Mortality of Pacific oyster Crassostrea gigas spat has increased considerably in Europe since 2008 linked to the spread of a variant of OsHV-1 called var. In the present study we demonstrated that O. edulis juveniles can be infected by OsHV-1 mu var when administered as an intramuscular injection. Mortality in the oysters injected with OsHV-1 mu var was first detected 4 days after injection and reached 25% mortality at day 10. Moreover, the high viral load observed and the detection of viral transcripts by in situ hybridization in several tissues of dying oysters suggested that OsHV-1 mu var was the cause of mortality in the O. edulis juveniles. This is therefore the first study to provide evidence about the pathogenicity of OsHV-1 var in a species that does not belong to the Crassostrea genus. Additionally, we present a novel method to detect OsHV-1 transcripts in infected individuals' using in situ hybridization. (C) 2016 Elsevier B.V. All rights reserved.
- Uncovering the immunological repertoire of the carpet shell clam Ruditapes decussatus through a transcriptomic-based approachPublication . Batista, Frederico; Churcher, Allison; Manchado, Manuel; Leitão, Alexandra; Power, DeborahThe grooved carpet-shell clam Ruditapes decussatus is native to the Northern Atlantic and Mediterranean Sea and has a high commercial value. It is one of the main native bivalve species cultured in Europe. The main objective of the present study was to gain further insights into the immunological repertoire of R. decussatus through a transcriptomic approach. Pooled mantle samples of eight R. decussatus individuals were sequenced using Illumina platform. A total of 67 132 contigs with more than 800 bp were obtained. Manual annotation of these contigs revealed 146 immune-related genes. The gene families in which the highest number of immune-related genes was observed were: C1q domain-containing proteins (63), tumor necrosis factors (15) and toll-like receptors (TLRs, 10). A total of 5 359 putative single nucleotide polymorphisms (SNPs) were identified in the 146 immune-related genes. The density of SNPs ranged between 0.04 and 7.92 SNPs/100 bp. The highest and the lowest SNP density were observed in genes of the C1q domain-containing protein family. Due to the importance of TLRs in innate immunity, we focused our attention on these membrane receptors. Ten TLRs were identified based on protein domain organization. Phylogenetic analysis revealed that R. decussatus TLRs were diverse and only 3 showed orthology with TLRs of known immune functions in other bivalve species. Moreover, our analysis suggests that lineage restricted-expansions of TLRs occurred in all mollusc taxa analysed including in venerids.
- Identification of molecular and physiological responses to chronic environmental challenge in an invasive species The Pacific oyster, Crassostrea gigasPublication . Clark, M. S.; Thorne, Michael A. S.; Araújo Amaral, Ana Margarida; Vieira, Florbela A.; Batista, Frederico; Reis, João; Power, DeborahUnderstanding the environmental responses of an invasive species is critical in predicting how ecosystem composition may be transformed in the future, especially under climate change. In this study, Crassostrea gigas, a species well adapted to the highly variable intertidal environment, was exposed to the chronic environmental challenges of temperature (19 and 24°C) and pH (ambient seawater and a reduction of 0.4 pH units) in an extended 3-month laboratory-based study. Physiological parameters were measured (condition index, shell growth, respiration, excretion rates, O:N ratios, and ability to repair shell damage) alongside molecular analyses. Temperature was by far the most important stressor, as demonstrated by reduced condition indexes and shell growth at 24°C, with relatively little effect detected for pH. Transcriptional profiling using candidate genes and SOLiD sequencing of mantle tissue revealed that classical “stress” genes, previously reported to be upregulated under acute temperature challenges, were not significantly expressed in any of the treatments, emphasizing the different response between acute and longer term chronic stress. The transcriptional profiling also elaborated on the cellular responses underpinning the physiological results, including the identification of the PI3K/AKT/mTOR pathway as a potentially novel marker for chronic environmental challenge. This study represents a first attempt to understand the energetic consequences of cumulative thermal stress on the intertidal C. gigas which could significantly impact on coastal ecosystem biodiversity and function in the future.
- Evidence of vertical transmission of ostreid herpesvirus 1 in the Portuguese oyster Crassostrea angulataPublication . Sanmartin, Monserrat Lopez; Power, Deborah; de la Herran, Roberto; Navas, José I.; Batista, FredericoIn order to determine if ostreid herpesvirus 1 (OsHV-1) can be vertically transmitted, 9 full-sib families of the Portuguese oyster Crassostrea angulata were produced using a factorial mating design with 3 males and 3 females. The parents were survivors from an OsHV-1 mortality outbreak. OsHV-1 DNA was not detected by conventional PCR in the mantle of parents, gametes or 3 day-old larvae. However, viral DNA was detected by real-time PCR in all gametes and larvae samples. These results show that C. angulata that have survived an OsHV-1 mortality outbreak can carry the virus and vertically transmit it to their offspring. (C) 2016 Elsevier Inc. All rights reserved.