Pedro M. Meirelles

Abrolhos Bank Reef Health Evaluated by Means of Water Quality, Microbial Diversity, Benthic Cover, and Fish Biomass Data

The health of the coral reefs of the Abrolhos Bank (southwestern Atlantic) was characterized with a holistic approach using measurements of four ecosystem components: (i) inorganic and organic nutrient concentrations, [1] fish biomass, [1] macroalgal and coral cover and (iv) microbial community composition and abundance. The possible benefits of protection from fishing were particularly evaluated by comparing sites with varying levels of protection. Two reefs within the well-enforced no-take area of the National Marine Park of Abrolhos (Parcel dos Abrolhos and California) were compared with two unprotected coastal reefs (Sebastião Gomes and Pedra de Leste) and one legally protected but poorly enforced coastal reef (the “paper park” of Timbebas Reef). The fish biomass was lower and the fleshy macroalgal cover was higher in the unprotected reefs compared with the protected areas. The unprotected and protected reefs had similar seawater chemistry. Lower vibrio CFU counts were observed in the fully protected area of California Reef. Metagenome analysis showed that the unprotected reefs had a higher abundance of archaeal and viral sequences and more bacterial pathogens, while the protected reefs had a higher abundance of genes related to photosynthesis. Similar to other reef systems in the world, there was evidence that reductions in the biomass of herbivorous fishes and the consequent increase in macroalgal cover in the Abrolhos Bank may be affecting microbial diversity and abundance. Through the integration of different types of ecological data, the present study showed that protection from fishing may lead to greater reef health. The data presented herein suggest that protected coral reefs have higher microbial diversity, with the most degraded reef (Sebastião Gomes) showing a marked reduction in microbial species richness. It is concluded that ecological conditions in unprotected reefs may promote the growth and rapid evolution of opportunistic microbial pathogens.

Metagenomic Analysis of Healthy and White Plague-Affected Mussismilia braziliensis Corals

Coral health is under threat throughout the world due to regional and global stressors. White plague disease (WP) is one of the most important threats affecting the major reef builder of the Abrolhos Bank in Brazil, the endemic coral Mussismilia braziliensis. We performed a metagenomic analysis of healthy and WP-affected M. braziliensis in order to determine the types of microbes associated with this coral species. We also optimized a protocol for DNA extraction from coral tissues. Our taxonomic analysis revealed Proteobacteria, Bacteroidetes, Firmicutes, Cyanobacteria, and Actinomycetes as the main groups in all healthy and WP-affected corals. Vibrionales, members of the Cytophaga–Flavobacterium–Bacteroides complex, Rickettsiales, and Neisseriales were more abundant in the WP-affected corals. Diseased corals also had more eukaryotic metagenomic sequences identified as Alveolata and Apicomplexa. Our results suggest that WP disease in M. braziliensis is caused by a polymicrobial consortium.

Physiologic and metagenomic attributes of the rhodoliths forming the largest CaCO3 bed in the South Atlantic Ocean.

Rhodoliths are free-living coralline algae (Rhodophyta, Corallinales) that are ecologically important for the functioning of marine environments. They form extensive beds distributed worldwide, providing a habitat and nursery for benthic organisms and space for fisheries, and are an important source of calcium carbonate. The Abrolhos Bank, off eastern Brazil, harbors the world’s largest continuous rhodolith bed (of ∼21 000 km2) and has one of the largest marine CaCO3 deposits (producing 25 megatons of CaCO3 per year). Nevertheless, there is a lack of information about the microbial diversity, photosynthetic potential and ecological interactions within the rhodolith holobiont. Herein, we performed an ecophysiologic and metagenomic analysis of the Abrolhos rhodoliths to understand their microbial composition and functional components. Rhodoliths contained a specific microbiome that displayed a significant enrichment in aerobic ammonia-oxidizing betaproteobacteria and dissimilative sulfate-reducing deltaproteobacteria. We also observed a significant contribution of bacterial guilds (that is, photolithoautotrophs, anaerobic heterotrophs, sulfide oxidizers, anoxygenic phototrophs and methanogens) in the rhodolith metagenome, suggested to have important roles in biomineralization. The increased hits in aromatic compounds, fatty acid and secondary metabolism subsystems hint at an important chemically mediated interaction in which a functional job partition among eukaryal, archaeal and bacterial groups allows the rhodolith holobiont to thrive in the global ocean. High rates of photosynthesis were measured for Abrolhos rhodoliths (52.16 μmol carbon m−2 s−1), allowing the entire Abrolhos rhodolith bed to produce 5.65 × 105 tons C per day. This estimate illustrates the great importance of the Abrolhos rhodolith beds for dissolved carbon production in the South Atlantic Ocean.

Baseline Assessment of Mesophotic Reefs of the Vitória-Trindade Seamount Chain Based on Water Quality, Microbial Diversity, Benthic Cover and Fish Biomass Data

Seamounts are considered important sources of biodiversity and minerals. However, their biodiversity and health status are not well understood; therefore, potential conservation problems are unknown. The mesophotic reefs of the Vitória-Trindade Seamount Chain (VTC) were investigated via benthic community and fish surveys, metagenomic and water chemistry analyses, and water microbial abundance estimations. The VTC is a mosaic of reef systems and includes fleshy algae dominated rhodolith beds, crustose coralline algae (CCA) reefs, and turf algae dominated rocky reefs of varying health levels. Macro-carnivores and larger fish presented higher biomass at the CCA reefs (4.4 kg per frame) than in the rhodolith beds and rocky reefs (0.0 to 0.1 kg per frame). A larger number of metagenomic sequences identified as primary producers (e.g., Chlorophyta and Streptophyta) were found at the CCA reefs. However, the rocky reefs contained more diseased corals (>90%) than the CCA reefs (~40%) and rhodolith beds (~10%). Metagenomic analyses indicated a heterotrophic and fast-growing microbiome in rocky reef corals that may possibly lead to unhealthy conditions possibly enhanced by environmental features (e.g. light stress and high loads of labile dissolved organic carbon). VTC mounts represent important hotspots of biodiversity that deserve further conservation actions.

Biological oxygen demand optode analysis of coral reef-associated microbial communities exposed to algal exudates

Algae-derived dissolved organic matter has been hypothesized to induce mortality of reef building corals. One proposed killing mechanism is a zone of hypoxia created by rapidly growing microbes. To investigate this hypothesis, biological oxygen demand (BOD) optodes were used to quantify the change in oxygen concentrations of microbial communities following exposure to exudates generated by turf algae and crustose coralline algae (CCA). BOD optodes were embedded with microbial communities cultured from Montastraea annularis and Mussismilia hispida, and respiration was measured during exposure to turf and CCA exudates. The oxygen concentrations along the optodes were visualized with a low-cost Submersible Oxygen Optode Recorder (SOOpR) system. With this system we observed that exposure to exudates derived from turf algae stimulated higher oxygen drawdown by the coral-associated bacteria than CCA exudates or seawater controls. Furthermore, in both turf and CCA exudate treatments, all microbial communities (coral-, algae-associated and pelagic) contributed significantly to the observed oxygen drawdown. This suggests that the driving factor for elevated oxygen consumption rates is the source of exudates rather than the initially introduced microbial community. Our results demonstrate that exudates from turf algae may contribute to hypoxia-induced coral stress in two different coral genera as a result of increased biological oxygen demand of the local microbial community. Additionally, the SOOpR system developed here can be applied to measure the BOD of any culturable microbe or microbial community.

Advanced microbial taxonomy combined with genome-based-approaches reveals that vibrio astriarenae sp. Nov., an agarolytic marine bacterium, forms a new clade in Vibrionaceae

Advances in genomic microbial taxonomy have opened the way to create a more universal and transparent concept of species but is still in a transitional stage towards becoming a defining robust criteria for describing new microbial species with minimum features obtained using both genome and classical polyphasic taxonomies. Here we performed advanced microbial taxonomies combined with both genome-based and classical approaches for new agarolytic vibrio isolates to describe not only a novel Vibrio species but also a member of a new Vibrio clade. Two novel vibrio strains (Vibrio astriarenae sp. nov. C7T and C20) showing agarolytic, halophilic and fermentative metabolic activity were isolated from a seawater sample collected in a coral reef in Okinawa. Intraspecific similarities of the isolates were identical in both sequences on the 16S rRNA and pyrH genes, but the closest relatives on the molecular phylogenetic trees on the basis of 16S rRNA and pyrH gene sequences were V. hangzhouensis JCM 15146T (97.8% similarity) and V. agarivorans CECT 5085T (97.3% similarity), respectively. Further multilocus sequence analysis (MLSA) on the basis of 8 protein coding genes (ftsZ, gapA, gyrB, mreB, pyrH, recA, rpoA, and topA) obtained by the genome sequences clearly showed the V. astriarenae strain C7T and C20 formed a distinct new clade protruded next to V. agarivorans CECT 5085T. The singleton V. agarivorans has never been included in previous MLSA of Vibrionaceae due to the lack of some gene sequences. Now the gene sequences are completed and analysis of 100 taxa in total provided a clear picture describing the association of V. agarivorans into pre-existing concatenated network tree and concluded its relationship to our vibrio strains. Experimental DNA-DNA hybridization (DDH) data showed that the strains C7T and C20 were conspecific but were separated from all of the other Vibrio species related on the basis of both 16S rRNA and pyrH gene phylogenies (e.g., V. agarivorans CECT 5085T, V. hangzhouensis JCM 15146T V. maritimus LMG 25439T, and V. variabilis LMG 25438T). In silico DDH data also supported the genomic relationship. The strains C7T also had less than 95% average amino acid identity (AAI) and average nucleotide identity (ANI) towards V. maritimus C210, V. variabilis C206, and V. mediterranei AK1T, V. brasiliensis LMG 20546T, V. orientalis ATCC 33934T, and V. sinaloensis DSM 21326. The name Vibrio astriarenae sp. nov. is proposed with C7 as the type strains. Both V. agarivorans CECT 5058T and V. astriarenae C7T are members of the newest clade of Vibrionaceae named Agarivorans.

Niche distribution and influence of environmental parameters in marine microbial communities: a systematic review

Associations between microorganisms occur extensively throughout Earth’s oceans. Understanding how microbial communities are assembled and how the presence or absence of species is related to that of others are central goals of microbial ecology. Here, we investigate co-occurrence associations between marine prokaryotes by combining 180 new and publicly available metagenomic datasets from different oceans in a large-scale meta-analysis. A co-occurrence network was created by calculating correlation scores between the abundances of microorganisms in metagenomes. A total of 1,906 correlations amongst 297 organisms were detected, segregating them into 11 major groups that occupy distinct ecological niches. Additionally, by analyzing the oceanographic parameters measured for a selected number of sampling sites, we characterized the influence of environmental variables over each of these 11 groups. Clustering organisms into groups of taxa that have similar ecology, allowed the detection of several significant correlations that could not be observed for the taxa individually.

Multiple Symbiodinium Strains Are Hosted by the Brazilian Endemic Corals Mussismilia spp.

Corals of genus Mussismilia (Mussidae) are one of the oldest extant clades of scleractinians. These Neogene relicts are endemic to the Brazilian coast and represent the main reef-building corals in the Southwest Atlantic Ocean (SAO). The relatively low-diversity/high-endemism SAO coralline systems are under rapid decline from emerging diseases and other local and global stressors, but have not been severely affected by coral bleaching. Despite the biogeographic significance and importance for understanding coral resilience, there is scant information about the diversity of Symbiodinium in this ocean basin. In this study, we established the first culture collections of Symbiodinium from Mussismilia hosts, comprising 11 isolates, four of them obtained by fluorescent-activated cell sorting (FACS). We also analyzed Symbiodinium diversity directly from Mussismilia tissue samples (N = 16) and characterized taxonomically the cultures and tissue samples by sequencing the dominant ITS2 region. Symbiodinium strains A4, B19, and C3 were detected. Symbiodinium C3 was predominant in the larger SAO reef system (Abrolhos), while Symbiodinium B19 was found only in deep samples from the oceanic Trindade Island. Symbiodinium strains A4 and C3 isolates were recovered from the same Mussismilia braziliensis coral colony. In face of increasing threats, these results indicate that Symbiodinium community dynamics shall have an important contribution for the resilience of Mussismilia spp. corals.

BaMBa: towards the integrated management of Brazilian marine environmental data

A new open access database, Brazilian Marine Biodiversity (BaMBa) (https://marinebiodiversity.lncc.br), was developed in order to maintain large datasets from the Brazilian marine environment. Essentially, any environmental information can be added to BaMBa. Certified datasets obtained from integrated holistic studies, comprising physical–chemical parameters, -omics, microbiology, benthic and fish surveys can be deposited in the new database, enabling scientific, industrial and governmental policies and actions to be undertaken on marine resources. There is a significant number of databases, however BaMBa is the only integrated database resource both supported by a government initiative and exclusive for marine data. BaMBa is linked to the Information System on Brazilian Biodiversity (SiBBr, http://www.sibbr.gov.br/) and will offer opportunities for improved governance of marine resources and scientists’ integration. Database URL: http://marinebiodiversity.lncc.br

Taxonomic and Functional Metagenomic Signature of Turfs in the Abrolhos Reef System (Brazil)

Turfs are widespread assemblages (consisting of microbes and algae) that inhabit reef systems. They are the most abundant benthic component in the Abrolhos reef system (Brazil), representing greater than half the coverage of the entire benthic community. Their presence is associated with a reduction in three-dimensional coral reef complexity and decreases the habitats available for reef biodiversity. Despite their importance, the taxonomic and functional diversity of turfs remain unclear. We performed a metagenomics and pigments profile characterization of turfs from the Abrolhos reefs. Turf microbiome primarily encompassed Proteobacteria (mean 40.57% ± s.d. 10.36, N = 1.548,192), Cyanobacteria (mean 35.04% ± s.d. 15.5, N = 1.337,196), and Bacteroidetes (mean 11.12% ± s.d. 4.25, N = 424,185). Oxygenic and anoxygenic phototrophs, chemolithotrophs, and aerobic anoxygenic phototrophic (AANP) bacteria showed a conserved functional trait of the turf microbiomes. Genes associated with oxygenic photosynthesis, AANP, sulfur cycle (S oxidation, and DMSP consumption), and nitrogen metabolism (N2 fixation, ammonia assimilation, dissimilatory nitrate and nitrite ammonification) were found in the turf microbiomes. Principal component analyses of the most abundant taxa and functions showed that turf microbiomes differ from the other major Abrolhos benthic microbiomes (i.e., corals and rhodoliths) and seawater. Taken together, these features suggest that turfs have a homogeneous functional core across the Abrolhos Bank, which holds diverse microbial guilds when comparing with other benthic organisms.