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Webster, N. S.

Publications and source records attributed to Webster, N. S..

10 recordsLinked to original sources

Thermal stress disrupts microbial symbiosis and host activity in the model sponge Ianthella basta

Climate change is threatening coral reef ecosystems around the world, causing significant declines in reef organisms, including sponges. The health of sponges is intimately linked to their symbiosis with microorganisms, yet little is known about their integrated response to ocean warming. Here, we present a comprehensive view of the effect of elevated sea surface temperatures (SST) on the model sponge Ianthella basta. I. basta individuals were exposed to temperatures up to 32 {degrees}C, 2-3 {degrees}C above the mean annual maxima. Host gene expression profiles showed an initial response to heat stress after 2 days, and a decreased expression of genes involved in maintaining tissue integrity, pumping capacity, vitamin transport, and stable symbioses after 4 to 8 days. Congruently, heat stressed samples started to show tissue regression and a reduced abundance of the dominant symbionts after 4 days. A significant loss of the symbionts occurred after 8 days, together with a reduction in microbially driven nitrogen cycling and amino-acid transport and an introduction of opportunistic microbes, which could lead to nutrient imbalance and further destabilisation of the holobiont. Together, this work provides important insights into the avenues through which future SST can impact host-microbe interactions in coral reef sponges.

microbiology↗

No-take marine reserves promote oligotrophic reef bacterioplankton communities across the Great Barrier Reef

Australias Great Barrier Reef is a biodiversity hotspot critical to ocean health, yet it faces increasing threats from climate change and localised impacts requiring effective conservation and management action. Rezoning of the Great Barrier Reef Marine Park in 2004 expanded No-Take Marine Reserves (NTMRs) to restrict extractive activities like fishing and collecting, creating one of the largest networks of marine reserves globally. Benefits like increased biomass of fisheries-targeted species and improved coral community health metrics have been reported, though the effects of zoning on water chemistry and seawater microbiology remain unexplored. Using data from the Great Barrier Reef Microbial Genomics Database, we investigated the structure of seawater microbiomes on 48 offshore reefs within NTMRs and fished reefs. A supervised classification method (MINT sPLS-DA) identified 350 indicator species that predict zoning with [~]71% accuracy (range 58-85%). Microbial communities broadly reflected reef states, with NTMR zones enriched in streamlined microbial oligotrophs (Pelagibacter and SAR86) correlating with higher cover of hard coral, crustose coralline algae, and herbivore fish abundance under lower nutrient conditions. By contrast, fished reefs harbored opportunists (Flavobacteriales, especially UA16, and Pseudomonadales) associating with elevated nutrients and turf algae cover. Co-occurrence networks revealed stronger competitive interactions in fished reefs, where nutrient-responsive taxa may outcompete other microbes, underscoring the need to investigate how these shifts influence reef nutrient cycling and function. Our findings reveal ecosystem-wide effects of marine zoning beyond fish protection, with distinct seawater microbiomes between fished reefs and NTMRs, which will help build decision tools for more targeted reef health monitoring assessments.

microbiology↗

An eco-evolutionary theory of host-associated microbiomes

Host-associated microbiomes often display host specificity and heritability, yet the evolutionary processes under which such structured communities first emerge are still unclear. In particular, the conditions by which intergenerational (i.e. vertical) transmission of microbes can evolve and generate host-specific microbiomes are still unresolved. Here, we present an eco-evolutionary theory of microbiome assembly under minimal assumptions of microbial dynamics (i.e. neutrally driven by environmental fluctuations) and host control. We consider the adaptive evolution of microbial and host traits, including microbiome size and vertical transmission. We show that environmental fluctuations can generate enough among-host microbial variation to enable host-level selection favouring beneficial microbiome configurations. Vertical transmission can then evolve and, even when weak, allow microbiome specificity to be inherited and amplified across generations despite continuous influx from the external environment. Selection is most effective at intermediate levels of environmental fluctuation and host lifespan, revealing fundamental trade-offs between stochastic assembly, inheritance, and dispersal of microbes. The resulting microbiomes are dense, host-specific, and heritable, yet retain high intraspecific variability and lack strict phylosymbiosis. Simulated patterns of microbial dominance, diversity, and host-microbiome dissimilarity closely match those observed in nature, as evidenced using marine sponge microbiomes. Our results provide a mechanistic theory for the early evolution of host-associated microbiomes, showing that beneficial and species-specific communities can arise through selection and inheritance prior to the evolution of dedicated host-control mechanisms.

evolutionary biology↗

Towards key principles of host-associated microbiome assembly

Symbiotic relationships between microbes and host organisms frequently involve the assembly of complex microbial communities (microbiomes) within hosts. Patterns at the community level influence life-history traits, the evolutionary trajectories of both microbes and their hosts, and are often critical for maintaining host health. These community-level patterns are dynamically driven by eco-evolutionary mechanisms acting at the individual level, such as microbial dispersal, host selection, and microbe-resource interactions. Critically, we still lack a clear picture of the ways in which these mechanisms interact to shape microbiome assembly. Here, we present a model of assembly to describe how distinct community structures can be characterised by underlying mechanisms. To illustrate the approach, we analyse microbiome data from marine sponges and simulate different structures of host-microbe associations, thereby bridging mechanistic models and empirical patterns. We further apply the model to human microbiome data to explore its relevance across biological systems, proposing that the combined effect of a small set of general mechanisms may govern diverse patterns of microbial diversity and abundance. Our findings advance ecological theory by linking individual-level processes to community-scale patterns, illuminating the key drivers underlying microbiome assembly.

microbiology↗

The planktonic microbiome of the Great Barrier Reef

Large genome databases have markedly improved our understanding of marine microorganisms. Although these resources have focused on prokaryotes, genomes from many dominant marine lineages, such as Pelagibacter and Prochlorococcus, are conspicuously underrepresented. Here, we present the Great Barrier Reef Microbial Genomes Database (GBR-MGD) comprising 5,283 prokaryotic genomes obtained from GBR seawater samples using Nanopore sequencing, including a collection of high quality genomes of underrepresented groups. We show that standard short read assemblies miss these populations due to a combination of strain heterogeneity and low GC% sequencing bias. The GBR-MGD also comprises 20 chromosome-level picoeukaryote and 808,585 viral genomes, including a newly described clade of marine Crassvirales. We demonstrate the use of the GBR-MGD to identify indicator taxa that can reliably predict the effects of reef management practices, such as the establishment of marine protected zones.

genomics↗

Taurine as a key intermediate for host-symbiont interaction in the tropical sponge Ianthella basta

Marine sponges are critical components of marine benthic fauna assemblages where their filter-feeding and reef-building capabilities provide bentho-pelagic coupling and crucial habitat. As potentially the oldest representation of a metazoan-microbe symbiosis, they also harbor dense, diverse, and species-specific communities of microbes, which are increasingly recognized for their contributions to dissolved organic matter (DOM) processing. Recent omics-based studies of marine sponge microbiomes have proposed numerous pathways of dissolved metabolite exchange between the host and symbionts within the context of the surrounding environment, but few studies have sought to experimentally interrogate these pathways. By using a combination of metaproteogenomics and laboratory incubations coupled with isotope-based functional assays, we showed that the dominant gammaproteobacterial symbiont Candidatus Taurinisymbion ianthellae residing in the marine sponge, Ianthella basta, expresses a pathway for the import and dissimilation of taurine, a ubiquitously occurring sulfonate metabolite in marine sponges. Candidatus Taurinisymbion ianthellae incorporates taurine-derived carbon and nitrogen while, at the same time, oxidizing the dissimilated sulfite into sulfate for export. Furthermore, we found that taurine-derived ammonia is exported by the symbiont for immediate oxidation by the dominant ammonia-oxidizing thaumarchaeal symbiont Candidatus Nitrosospongia ianthellae. Metaproteogenomic analyses also indicate that Candidatus Taurinisymbion ianthellae likely imports DMSP and possesses both pathways for DMSP demethylation and cleavage, enabling it to use this compound as a carbon and sulfur source for biomass, as well as for energy conservation. These results highlight the important role of biogenic sulfur compounds in the interplay between Ianthella basta and its microbial symbionts.

microbiology↗

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species due to simulated future conditions of ocean warming and acidification

The symbiotic relationship between coral and its endosymbiotic algae, Symbiodiniaceae, greatly influences the hosts potential to withstand environmental stress. To date, the effects of climate change on this relationship has primarily focused on adult corals. Uncovering the effects of environmental stress on the establishment and development of this symbiosis in early life stages is critical for predicting how corals may respond to climate change. To determine the impacts of future climate projections on the establishment of symbionts in juvenile corals, ITS2 amplicon sequencing of single coral juveniles was applied to Goniastrea retiformis and Acropora millepora before and after exposure to three climate conditions of varying temperature and pCO2 levels (current and RCP8.5 in 2050 and 2100). Compared to ambient conditions, juvenile corals experienced shuffling in the relative abundance of Cladocopium (C1m, reduction) to Durusdinium (D1 and D1a, increase) over time. We calculated a novel risk metric incorporating functional redundancy and likelihood of impact on host physiology to identify the loss of D1a as a low risk to the coral compared to the loss of "higher risk" taxa like D1 and C1m. Although the increase in stress tolerant Durusdinium under future warming was encouraging for A. millepora, by 2100, G. retiformis communities displayed signs of symbiosis de-regulation, suggesting this acclimatory mechanism may have species-specific thresholds. These results emphasize the need for understanding of long-term effects of climate change induced stress on coral juveniles and their potential for increased acclimation to heat tolerance through changes in symbiosis. Originality StatementHere we assessed changes in the uptake and establishment of Symbiodiniaceae in the early lifehistory stages of two coral species under future climate scenarios. Our study represents the first such assessment of future climate change projections (increased temperature and pCO2) influencing Symbiodiniaceae acquisition and specifically shows a community structure dominated by the stress tolerant genus Durusdinium. We also develop a novel risk metric that includes taxonomic function and redundancy to estimate the impact of symbiont taxa changes on coral physiology. Through the risk metric, we relate the stress-induced changes in symbiont community structure to the likelihood of functional loss to better understand the extent to which these changes may lead to a decrease in coral health.

ecology↗

Novel reference transcriptomes for the sponges Carteriospongia foliascens and Cliona orientalis and associated algal symbiont Gerakladium endoclionum

Transcriptomes from sponges are important resources for studying the stress responses of these ecologically important filter feeders, the interactions between sponges and their symbionts, and the evolutionary history of metazoans. Here, we generated reference transcriptomes for two common and cosmopolitan Indo-Pacific sponge species: Carteriospongia foliascens and Cliona orientalis. We also created a reference transcriptome for the primary symbiont of C. orientalis - Gerakladium endoclionum. To ensure a full repertoire of transcripts were included, clones of each sponge species were exposed to a range of individual stressors: decreased salinity, elevated temperature, elevated suspended sediment concentrations, sediment deposition and light attenuation. RNA extracted from all treatments was pooled for each species, using equal concentrations from each clone. Sequencing of pooled RNA yielded 409 and 418 million raw reads for C. foliascens and C. orientalis holobionts (host and symbionts), respectively. Reads underwent quality trimming before assembly with Trinity. Assemblies were filtered into sponge-specific or, for G. endoclionum, symbiont-specific assemblies. Assemblies for C. foliascens, C. orientalis, and G. endoclionum contained 67,304, 82,895, and 28,670 contigs, respectively. Contigs represented 15,248-37,344 isogroups ([~]genes) per assembly, and N50s ranged 1,672-4,355 bp. Gene ortholog analysis verified a high level of completeness and quality for sponge-specific transcriptomes, with an average 93% of core EuKaryotic Orthologous Groups (KOGs) and 98% of single-copy metazoan core gene orthologs identified. The G. endoclionum assembly was partial with only 56% of core KOGs and 32% of single-copy eukaryotic core gene orthologs identified. These reference transcriptomes are a valuable resource for future molecular research aimed at assessing sponge stress responses.

zoology↗

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical sponge Ianthella basta

Marine sponges represent one of the few eukaryotic groups that frequently harbor symbiotic members of the Thaumarchaeota, which are important chemoautotrophic ammonia-oxidizers in many environments. However, in most studies, direct demonstration of ammonia-oxidation by these archaea within sponges is lacking, and little is known about sponge-specific adaptations of ammonia-oxidizing archaea (AOA). Here, we characterized the thaumarchaeal symbiont of the marine sponge Ianthella basta using metaproteogenomics, fluorescence in situ hybridization, qPCR and isotope-based functional assays. "Candidatus Nitrosospongia bastadiensis" is only distantly related to cultured AOA. It is an abundant symbiont that is solely responsible for nitrite formation from ammonia in I. basta that surprisingly does not harbor nitrite-oxidizing microbes. Furthermore, this AOA is equipped with an expanded set of extracellular subtilisin-like proteases, a metalloprotease unique among archaea, as well as a putative branched-chain amino acid ABC transporter. This repertoire is strongly indicative of a mixotrophic lifestyle and is (with slight variations) also found in other sponge-associated, but not in free-living AOA. We predict that this feature as well as an expanded and unique set of secreted serpins (protease inhibitors), a unique array of eukaryotic-like proteins, and a DNA-phosporothioation system, represent important adaptations of AOA to life within these ancient filter-feeding animals. Originality-Significance StatementMany marine sponges harbor symbiotic members of the Thaumarchaeota, but there is generally only indirect evidence available about their functional role within these filter-feeding animals. Furthermore, the specific adaptations of thaumarchaeal symbionts to their sponge hosts are incompletely understood. In this study, we thoroughly characterized a thaumarchaeal symbiont residing in the reef sponge Ianthella basta and demonstrate by using a combination of molecular tools and isotope techniques, that it is the only ammonia-oxidizer in its host. In contrast to other sponges, I. basta does not contain nitrite-oxidizing microbes and thus excretes considerable amounts of nitrite. Furthermore, using metagenomics and metaproteomics we reveal important adaptations of this symbiont, that represents a new genus within the Thaumarchaeota, and conclude that it most likely lives as a mixotroph in its sponge host.

microbiology↗

Microbial predictors of environmental perturbations in coral reef ecosystems

Incorporation of microbial community data into environmental monitoring programs could improve prediction and management of environmental pressures. Coral reefs have experienced dramatic declines due to cumulative impacts of local and global stressors. Here we assess the utility of free-living (i.e. seawater and sediment) and host-associated (i.e. corals, sponges and macroalgae) microbiomes for diagnosing environmental perturbation based on their habitat-specificity, environmental sensitivity and uniformity. We show that the seawater microbiome has the greatest diagnostic value, with environmental parameters explaining 56% of the observed compositional variation and temporal successions being dominated by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less affected by the environment and their community assembly patterns were generally less uniform. Further, seawater microbial community data provided an accurate prediction on the environmental state, highlighting the diagnostic value of microorganisms and illustrating how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater.\n\nImportanceThe recent success in disease diagnostics based on the human microbiome has highlighted the utility of this approach for model systems. However, despite improved prediction and management of environmental pressures from the inclusion of microbial community data in monitoring programs, this approach has not previously been applied to coral reef ecosystems. Coral reefs are facing unprecedented pressure on a local and global scale, and sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. In this study, we performed the first assessment of the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems. Our results reveal that free-living microbial communities have a higher potential to infer environmental parameters than host-associated microbial communities due to their higher determinacy and environmental sensitivity. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.

microbiology↗