School of BioSciences - Research Publications
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ItemA targeted approach to enrich host-associated bacteria for metagenomic sequencing.(Oxford University Press (OUP), 2024)Multicellular eukaryotic organisms are hosts to communities of bacteria that reside on or inside their tissues. Often the eukaryotic members of the system contribute to high proportions of metagenomic sequencing reads, making it challenging to achieve sufficient sequencing depth to evaluate bacterial ecology. Stony corals are one such complex community; however, separation of bacterial from eukaryotic (primarily coral and algal symbiont) cells has so far not been successful. Using a combination of hybridization chain reaction fluorescence in situ hybridization and fluorescence activated cell sorting (HCR-FISH + FACS), we sorted two populations of bacteria from five genotypes of the coral Acropora loripes, targeting (i) Endozoicomonas spp, and (ii) all other bacteria. NovaSeq sequencing resulted in 67-91 M reads per sample, 55%-90% of which were identified as bacterial. Most reads were taxonomically assigned to the key coral-associated family, Endozoicomonadaceae, with Vibrionaceae also abundant. Endozoicomonadaceae were 5x more abundant in the 'Endozoicomonas' population, highlighting the success of the dual-labelling approach. This method effectively enriched coral samples for bacteria with <1% contamination from host and algal symbionts. The application of this method will allow researchers to decipher the functional potential of coral-associated bacteria. This method can also be adapted to accommodate other host-associated communities.
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ItemTissue-associated and vertically transmitted bacterial symbiont in the coral Pocillopora acuta(OXFORD UNIV PRESS, 2024-01-08)Coral microhabitats are colonized by a myriad of microorganisms, including diverse bacteria which are essential for host functioning and survival. However, the location, transmission, and functions of individual bacterial species living inside the coral tissues remain poorly studied. Here, we show that a previously undescribed bacterial symbiont of the coral Pocillopora acuta forms cell-associated microbial aggregates (CAMAs) within the mesenterial filaments. CAMAs were found in both adults and larval offspring, suggesting vertical transmission. In situ laser capture microdissection of CAMAs followed by 16S rRNA gene amplicon sequencing and shotgun metagenomics produced a near complete metagenome-assembled genome. We subsequently cultured the CAMA bacteria from Pocillopora acuta colonies, and sequenced and assembled their genomes. Phylogenetic analyses showed that the CAMA bacteria belong to an undescribed Endozoicomonadaceae genus and species, which we propose to name Candidatus Sororendozoicomonas aggregata gen. nov sp. nov. Metabolic pathway reconstruction from its genome sequence suggests this species can synthesize most amino acids, several B vitamins, and antioxidants, and participate in carbon cycling and prey digestion, which may be beneficial to its coral hosts. This study provides detailed insights into a new member of the widespread Endozoicomonadaceae family, thereby improving our understanding of coral holobiont functioning. Vertically transmitted, tissue-associated bacteria, such as Sororendozoicomonas aggregata may be key candidates for the development of microbiome manipulation approaches with long-term positive effects on the coral host.
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ItemDNA from non-viable bacteria biases diversity estimates in the corals Acropora loripes and Pocillopora acuta(BMC, 2023-12-08)BACKGROUND: Nucleic acid-based analytical methods have greatly expanded our understanding of global prokaryotic diversity, yet standard metabarcoding methods provide no information on the most fundamental physiological state of bacteria, viability. Scleractinian corals harbour a complex microbiome in which bacterial symbionts play critical roles in maintaining health and functioning of the holobiont. However, the coral holobiont contains both dead and living bacteria. The former can be the result of corals feeding on bacteria, rapid swings from hyper- to hypoxic conditions in the coral tissue, the presence of antimicrobial compounds in coral mucus, and an abundance of lytic bacteriophages. RESULTS: By combining propidium monoazide (PMA) treatment with high-throughput sequencing on six coral species (Acropora loripes, A. millepora, A. kenti, Platygyra daedalea, Pocillopora acuta, and Porites lutea) we were able to obtain information on bacterial communities with little noise from non-viable microbial DNA. Metabarcoding of the 16S rRNA gene showed significantly higher community evenness (85%) and species diversity (31%) in untreated compared with PMA-treated tissue for A. loripes only. While PMA-treated coral did not differ significantly from untreated samples in terms of observed number of ASVs, > 30% of ASVs were identified in untreated samples only, suggesting that they originated from cell-free/non-viable DNA. Further, the bacterial community structure was significantly different between PMA-treated and untreated samples for A. loripes and P. acuta indicating that DNA from non-viable microbes can bias community composition data in coral species with low bacterial diversity. CONCLUSIONS: Our study is highly relevant to microbiome studies on coral and other host organisms as it delivers a solution to excluding non-viable DNA in a complex community. These results provide novel insights into the dynamic nature of host-associated microbiomes and underline the importance of applying versatile tools in the analysis of metabarcoding or next-generation sequencing data sets.
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ItemHeat-evolved microalgal symbionts increase thermal bleaching tolerance of coral juveniles without a trade-off against growth(SPRINGER, 2023-12)Abstract Global climate change is threatening the persistence of coral reefs as associated summer heatwaves trigger the loss of microalgal endosymbionts (Symbiodiniaceae) from the coral tissues, or coral bleaching. We infected aposymbiotic juveniles of the coral Acropora tenuis with either wildtype (WT10) or heat-evolved (SS1 or SS8) Symbiodiniaceae strains Cladocopium proliferum (formerly referred to as Cladocopium goreaui and Cladocopium C1acro). After 10 months at 27 °C, SS8-juveniles were 2 × larger than SS1- or WT10-juveniles. In response to a simulated heatwave (31 °C for 41 days), the WT10-juveniles bleached and showed a decline in respiration while cell densities and respiration in both SS-juvenile groups remained unchanged compared to the controls. These results reveal that some heat-evolved strains can increase the bleaching tolerance of juvenile corals without a trade-off against growth. This response is opposite to the lower nutrient provisioning often reported for naturally thermotolerant Symbiodiniaceae (e.g. genus Durusdinium), thereby offering enhanced fitness to the host without the ecological consequences of diminished growth.
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ItemInoculation with Roseovarius increases thermal tolerance of the coral photosymbiont, Breviolum minutum(FRONTIERS MEDIA SA, 2023-08-10)Coral reefs are diverse marine ecosystems that have tremendous ecological and cultural value and support more than 25% of eukaryote marine biodiversity. Increased ocean temperatures and light intensity trigger coral bleaching, the breakdown of the relationship between corals and their photosymbionts, dinoflagellates of the family Symbiodiniaceae. This leaves corals without their primary energy source, thereby leading to starvation and, often, death. Coral bleaching is hypothesized to occur due to an overproduction of reactive oxygen species (ROS) by Symbiodiniaceae, which subsequently accumulate in coral tissues. Bacterial probiotics have been proposed as an approach to mitigate coral bleaching, by reducing ROS levels in the coral holobiont through bacterial antioxidant production. Both corals and Symbiodiniaceae are known to associate with bacteria. However, the Symbiodiniaceae-bacteria relationship, and its impact on Symbiodiniaceae thermal tolerance, remains a poorly studied area. In this study, cultured Symbiodiniaceae of the species Breviolum minutum were treated with antibiotics to reduce their bacterial load. The cultures were subsequently inoculated with bacterial isolates from the genus Roseovarius that were isolated from the same B. minutum culture and showed either high or low ROS-scavenging abilities. The B. minutum cultures were then exposed to experimental heat stress for 16 days, and their health was monitored through measurements of cell density and photochemical efficiency of photosystem II. It was found that B. minutum inoculated with Roseovarius with higher ROS-scavenging abilities showed greater cell growth at elevated temperatures, compared to cultures inoculated with a Roseovarius strain with lower ROS-scavenging abilities. This suggests that Roseovarius may play a role in Symbiodiniaceae fitness at elevated temperatures. Analysis of Symbiodiniaceae-associated bacterial communities through 16S rRNA gene metabarcoding revealed that Roseovarius relative abundance increased in B. minutum cultures following inoculation and with elevated temperature exposure, highlighting the contribution they may have in shielding B. minutum from thermal stress, although other bacterial community changes may have also contributed to these observations. This study begins to unpick the relationship between Symbiodiniaceae and their bacteria and opens the door for the use of Symbiodiniaceae-associated bacteria in coral reef conservation approaches.
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ItemNo Preview AvailableFunctional potential and evolutionary response to long-term heat selection of bacterial associates of coral photosymbionts(AMER SOC MICROBIOLOGY, 2023-12-21)Symbiotic microorganisms are crucial for the survival of corals and their resistance to coral bleaching in the face of climate change. However, the impact of microbe-microbe interactions on coral functioning is mostly unknown but could be essential factors for coral adaption to future climates. Here, we investigated interactions between cultured dinoflagellates of the Symbiodiniaceae family, essential photosymbionts of corals, and associated bacteria. By assessing the genomic potential of 49 bacteria, we found that they are likely beneficial for Symbiodiniaceae, through the production of B vitamins and antioxidants. Additionally, bacterial genes involved in host-symbiont interactions, such as secretion systems, accumulated mutations following long-term exposure to heat, suggesting symbiotic interactions may change under climate change. This highlights the importance of microbe-microbe interactions in coral functioning.
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ItemNo Preview AvailableGenomic exploration of coral-associated bacteria: identifying probiotic candidates to increase coral bleaching resilience in Galaxea fascicularis(BMC, 2023-08-19)BACKGROUND: Reef-building corals are acutely threatened by ocean warming, calling for active interventions to reduce coral bleaching and mortality. Corals associate with a wide diversity of bacteria which can influence coral health, but knowledge of specific functions that may be beneficial for corals under thermal stress is scant. Under the oxidative stress theory of coral bleaching, bacteria that scavenge reactive oxygen (ROS) or nitrogen species (RNS) are expected to enhance coral thermal resilience. Further, bacterial carbon export might substitute the carbon supply from algal photosymbionts, enhance thermal resilience and facilitate bleaching recovery. To identify probiotic bacterial candidates, we sequenced the genomes of 82 pure-cultured bacteria that were isolated from the emerging coral model Galaxea fascicularis. RESULTS: Genomic analyses showed bacterial isolates were affiliated with 37 genera. Isolates such as Ruegeria, Muricauda and Roseovarius were found to encode genes for the synthesis of the antioxidants mannitol, glutathione, dimethylsulfide, dimethylsulfoniopropionate, zeaxanthin and/or β-carotene. Genes involved in RNS-scavenging were found in many G. fascicularis-associated bacteria, which represents a novel finding for several genera (including Pseudophaeobacter). Transporters that are suggested to export carbon (semiSWEET) were detected in seven isolates, including Pseudovibrio and Roseibium. Further, a range of bacterial strains, including strains of Roseibium and Roseovarius, revealed genomic features that may enhance colonisation and association of bacteria with the coral host, such as secretion systems and eukaryote-like repeat proteins. CONCLUSIONS: Our work provides an in-depth genomic analysis of the functional potential of G. fascicularis-associated bacteria and identifies novel combinations of traits that may enhance the coral's ability to withstand coral bleaching. Identifying and characterising bacteria that are beneficial for corals is critical for the development of effective probiotics that boost coral climate resilience. Video Abstract.
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ItemNo Preview AvailableHeat-evolved algal symbionts enhance bleaching tolerance of adult corals without trade-off against growth(WILEY, 2023-12)Ocean warming has caused coral mass bleaching and mortality worldwide and the persistence of symbiotic reef-building corals requires rapid acclimation or adaptation. Experimental evolution of the coral's microalgal symbionts followed by their introduction into coral is one potential method to enhance coral thermotolerance. Heat-evolved microalgal symbionts of the generalist species, Cladocopium proliferum (strain SS8), were exposed to elevated temperature (31°C) for ~10 years, and were introduced into four genotypes of chemically bleached adult fragments of the scleractinian coral, Galaxea fascicularis. Two of the four coral genotypes acquired SS8. The new symbionts persisted for the 5 months of the experiment and enhanced adult coral thermotolerance, compared with corals that were inoculated with the wild-type C. proliferum strain. Thermotolerance of SS8-corals was similar to that of coral fragments from the same colony hosting the homologous symbiont, Durusdinium sp., which is naturally heat tolerant. However, SS8-coral fragments exhibited faster growth and recovered cell density and photochemical efficiency more quickly following chemical bleaching and inoculation under ambient temperature relative to Durusdinium-corals. Mass spectrometry imaging suggests that algal pigments involved in photobiology and oxidative stress were the greatest contributors to the thermotolerance differences between coral hosting heat-evolved versus wild-type C. proliferum. These pigments may have increased photoprotection in the heat-evolved symbionts. This is the first laboratory study to show that thermotolerance of adult corals (G. fascicularis) can be enhanced via the uptake of exogenously supplied, heat-evolved symbionts, without a trade-off against growth under ambient temperature. Importantly, heat-evolved C. proliferum remained in the corals in moderate abundance 2 years after first inoculation, suggesting long-term stability of this novel symbiosis and potential long-term benefits to coral thermotolerance.
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ItemNo Preview AvailableChemical mutagenesis and thermal selection of coral photosymbionts induce adaptation to heat stress with trait trade-offs(WILEY, 2023-09)Despite the relevance of heat-evolved microalgal endosymbionts to coral reef restoration, to date, few Symbiodiniaceae strains have been thermally enhanced via experimental evolution. Here, we investigated whether the thermal tolerance of Symbiodiniaceae can be increased through chemical mutagenesis followed by thermal selection. Strains of Durusdinium trenchii, Fugacium kawagutii and Symbiodinium pilosum were exposed to ethyl methanesulfonate to induce random mutagenesis, and then underwent thermal selection at high temperature (31/33°C). After 4.6-5 years of experimental evolution, the in vitro thermal tolerance of these strains was assessed via reciprocal transplant experiments to ambient (27°C) and elevated (31/35°C) temperatures. Growth, photosynthetic efficiency, oxidative stress and nutrient use were measured to compare thermal tolerance between strains. Heat-evolved D. trenchii, F. kawagutii and S. pilosum strains all exhibited increased photosynthetic efficiency under thermal stress. However, trade-offs in growth rates were observed for the heat-evolved D. trenchii lineage at both ambient and elevated temperatures. Reduced phosphate and nitrate uptake rates in F. kawagutii and S. pilosum heat-evolved lineages, respectively, suggest alterations in nutrition resource usage and allocation processes may have occurred. Increased phosphate uptake rates of the heat-evolved D. trenchii strain indicate that experimental evolution resulted in further trade-offs in this species. These findings deepen our understanding of the physiological responses of Symbiodiniaceae cultures to thermal selection and their capacity to adapt to elevated temperatures. The new heat-evolved Symbiodiniaceae developed here may be beneficial for coral reef restoration efforts if their enhanced thermal tolerance can be conferred in hospite.
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ItemNo Preview AvailableSelecting coral species for reef restoration(WILEY, 2023-08-01)Abstract Humans have long sought to restore species but little attention has been directed at how to best select a subset of foundation species for maintaining rich assemblages that support ecosystems, like coral reefs and rainforests, which are increasingly threatened by environmental change. We propose a two‐part hedging approach that selects optimized sets of species for restoration. The first part acknowledges that biodiversity supports ecosystem functions and services, and so it ensures precaution against loss by allocating an even spread of phenotypic traits. The second part maximizes species and ecosystem persistence by weighting species based on characteristics that are known to improve ecological persistence—for example abundance, species range and tolerance to environmental change. Using existing phenotypic‐trait and ecological data for reef building corals, we identified sets of ecologically persistent species by examining marginal returns in occupancy of phenotypic trait space. We compared optimal sets of species with those from the world's southern‐most coral reef, which naturally harbours low coral diversity, to show these occupy much of the trait space. Comparison with an existing coral restoration program indicated that current corals used for restoration only cover part of the desired trait space and programs may be improved by including species with different traits. Synthesis and applications. While there are many possible criteria for selecting species for restoration, the approach proposed here addresses the need to insure against unpredictable losses of ecosystem services by focusing on a wide range of phenotypic traits and ecological characteristics. Furthermore, the flexibility of the approach enables the functional goals of restoration to vary depending on environmental context, stakeholder values, and the spatial and temporal scales at which meaningful impacts can be achieved.