Deep sea treasures - Insights from museum archives shed light on coral microbial diversity within deepest ocean ecosystems.

Deep sea benthic habitats are low productivity ecosystems that host an abundance of organisms within the Cnidaria phylum. The technical limitations and the high cost of deep sea surveys have made exploring deep sea environments and the biology of the organisms that inhabit them challenging. In spite of the widespread recognition of Cnidaria's environmental importance in these ecosystems, the microbial assemblage and its role in coral functioning have only been studied for a few deep water corals. Here, we explored the microbial diversity of deep sea corals by recovering nucleic acids from museum archive specimens. Firstly, we amplified and sequenced the V1-V3 regions of the 16S rRNA gene of these specimens, then we utilized the generated sequences to shed light on the microbial diversity associated with seven families of corals collected from depth in the Coral Sea (depth range 1309 to 2959 m) and Southern Ocean (depth range 1401 to 2071 m) benthic habitats. Surprisingly, Cyanobacteria sequences were consistently associated with six out of seven coral families from both sampling locations, suggesting that these bacteria are potentially ubiquitous members of the microbiome within these cold and deep sea water corals. Additionally, we show that Cnidaria might benefit from symbiotic associations with a range of chemosynthetic bacteria including nitrite, carbon monoxide and sulfur oxidizers. Consistent with previous studies, we show that sequences associated with the bacterial phyla Proteobacteria, Verrucomicrobia, Planctomycetes and Acidobacteriota dominated the microbial community of corals in the deep sea. We also explored genomes of the bacterial genus Mycoplasma, which we identified as associated with specimens of three deep sea coral families, finding evidence that these bacteria may aid the host immune system. Importantly our results show that museum specimens retain components of host microbiome that can provide new insights into the diversity of deep sea coral microbiomes (and potentially other organisms), as well as the diversity of microbes writ large in deep sea ecosystems.

Spatial extent of dysbiosis in the branching coral Pocillopora damicornis during an acute disease outbreak.

Globally, coral reefs face increasing disease prevalence and large-scale outbreak events. These outbreaks offer insights into microbial and functional patterns of coral disease, including early indicators of disease that may be present in visually-healthy tissues. Outbreak events also allow investigation of how reef-building corals, typically colonial organisms, respond to disease. We studied Pocillopora damicornis during an acute tissue loss disease outbreak on Guam to determine whether dysbiosis was present in visually-healthy tissues ahead of advancing disease lesions. These data reveal that coral fragments with visual evidence of disease are expectedly dysbiotic with high microbial and metabolomic variability. However, visually-healthy tissues from the same colonies lacked dysbiosis, suggesting disease containment near the affected area. These results challenge the idea of using broad dysbiosis as a pre-visual disease indicator and prompt reevaluation of disease assessment in colonial organisms such as reef-building corals.

The impact of rising temperatures on the prevalence of coral diseases and its predictability: A global meta-analysis.

Coral reefs are under threat from disease as climate change alters environmental conditions. Rising temperatures exacerbate coral disease, but this relationship is likely complex as other factors also influence coral disease prevalence. To better understand this relationship, we meta-analytically examined 108 studies for changes in global coral disease over time alongside temperature, expressed using average summer sea surface temperature (SST) and cumulative heat stress as weekly sea surface temperature anomalies (WSSTAs). We found that both rising average summer SST and WSSTA were associated with global increases in the mean and variability in coral disease prevalence. Global coral disease prevalence tripled, reaching 9.92% in the 25 years examined, and the effect of 'year' became more stable (i.e. prevalence has lower variance over time), contrasting the effects of the two temperature stressors. Regional patterns diverged over time and differed in response to average summer SST. Our model predicted that, under the same trajectory, 76.8% of corals would be diseased globally by 2100, even assuming moderate average summer SST and WSSTA. These results highlight the need for urgent action to mitigate coral disease. Mitigating the impact of rising ocean temperatures on coral disease is a complex challenge requiring global discussion and further study.

A coral disease outbreak highlights vulnerability of remote high-latitude lagoons to global and local stressors.

Outbreaks of coral disease are often associated with global and local stressors like changes in temperature and poor water quality. A severe coral disease outbreak was recorded in the primary reef-building taxa Montipora spp. in a high-latitude lagoon at Norfolk Island following heat stress and pollution events in 2020. Disease signs suggest the occurrence of a Montiporid White Syndrome with four distinct phases and maximum measured tissue loss of 329 mm-2 day-1. In December 2020 and April 2021, 60% of the Montipora community were impacted and disease severity increased by 54% over this period. Spatial patterns in prevalence indicate the disease is associated with exposure to poor water quality in addition to size class of coral colonies. High prevalence levels make this event comparable to some of the most severe coral disease outbreaks recorded to date demonstrating the vulnerability of this system to combined impacts of warming and pollution.

Intestinal Microbiome Richness of Coral Reef Damselfishes (Actinopterygii: Pomacentridae).

Fish gastro-intestinal system harbors diverse microbiomes that affect the host's digestion, nutrition, and immunity. Despite the great taxonomic diversity of fish, little is understood about fish microbiome and the factors that determine its structure and composition. Damselfish are important coral reef species that play pivotal roles in determining algae and coral population structures of reefs. Broadly, damselfish belong to either of two trophic guilds based on whether they are planktivorous or algae-farming. In this study, we used 16S rRNA gene sequencing to investigate the intestinal microbiome of 5 planktivorous and 5 algae-farming damselfish species (Pomacentridae) from the Great Barrier Reef. We detected Gammaproteobacteria ASVs belonging to the genus Actinobacillus in 80% of sampled individuals across the 2 trophic guilds, thus, bacteria in this genus can be considered possible core members of pomacentrid microbiomes. Algae-farming damselfish had greater bacterial alpha-diversity, a more diverse core microbiome and shared 35 ± 22 ASVs, whereas planktivorous species shared 7 ± 3 ASVs. Our data also highlight differences in microbiomes associated with both trophic guilds. For instance, algae-farming damselfish were enriched in Pasteurellaceae, whilst planktivorous damselfish in Vibrionaceae. Finally, we show shifts in bacterial community composition along the intestines. ASVs associated with the classes Bacteroidia, Clostridia, and Mollicutes bacteria were predominant in the anterior intestinal regions while Gammaproteobacteria abundance was higher in the stomach. Our results suggest that the richness of the intestinal bacterial communities of damselfish reflects host species diet and trophic guild.

O sistema gastro-intestinal de peixes abriga microbiomas diversos que afetam a digestão, nutrição e imunidade do hospedeiro. Apesar da grande diversidade taxonômica dos peixes, entende-se pouco sobre o microbioma dos peixes e fatores que determinam sua estrutura e composição. Peixes-donzela são espécies importantes em recifes de coral que exercem papéis pivotais na determinação da estrutura de algas e corais dos recifes. De forma geral, peixes-donzela pertencem à uma de duas guildas tróficas dependendo se são planctívoros ou algívoros. Nesse estudo, usamos sequenciamento do gene 16S rRNA para investigar o microbioma intestinal de cinco espécies planctívoras e cinco espécies algívoras de peixes-donzela (Pomacentridae) da Grande Barreira de Corais. Detectamos ASVs de Gammaproteobacteria pertencendo ao gênero Actinobacillus em 80% dos indivíduos amostrados nas duas guildas tróficas, logo, bactérias desse gênero podem ser consideradas como possíveis membros essenciais do microbioma dos pomacentrídeos. Peixes-donzela algívoros apresentaram uma maior alpha-diversidade bacteriana, um microbioma essencial mais diverso e compartilharam 35 ± 22 ASVs, e espécies planctívoras compartilharam 7 ± 3 ASVs. Nossos dados também ilustram diferenças nos microbiomas associados com ambas guildas tróficas. Por exemplo, peixes-donzela algívoros estavam enriquecidos em Pasteurellaceae, enquanto peixes-donzela planctívoros, em Vibrionaceae. Finalmente, demonstramos mudanças na composição da comunidade bacteriana associada com as classes Bacteroidia, Clostridia e Mollicutes foram predominantes nas regiões intestinais anteriores enquanto a abundância de Gammaproteobacteria foi maior no estômago. Nossos resultados sugerem que a riqueza das comunidades bacterianas intestinais de peixes-donzela refletem a dieta da espécie do hospedeiro, bem como a sua guilda trófica.

Bleaching Susceptibility and Resistance of Octocorals and Anemones at the World's Southern-Most Coral Reef.

Coral reefs are amongst the most biodiverse ecosystems on earth, and while stony corals create the foundational complexity of these ecosystems, octocorals and anemones contribute significantly to their biodiversity and function. Like stony corals, many octocorals contain Symbiodiniaceae endosymbionts and can bleach when temperatures exceed the species' upper thermal limit. Here, we report octocoral bleaching susceptibility and resistance within the subtropical Lord Howe Island coral reef ecosystem during and after marine heatwaves in 2019. Octocoral and anemone surveys were conducted at multiple reef locations within the Lord Howe Island lagoon during, immediately after, and 7 months after the heatwaves. One octocoral species, Cladiella sp. 1, experienced bleaching and mortality, with some bleached colonies detaching from the reef structure during the heatwave (presumed dead). Those that remained attached to the benthos survived the event and recovered endosymbionts within 7 months of bleaching. Cladiella sp. 1 Symbiodiniaceae density (in cells per µg protein), chlorophyll a and c 2 per µg protein, and photosynthetic efficiency were significantly lower in bleached colonies compared to unbleached colonies, while chlorophyll a and c 2 per symbiont were higher. Interestingly, no other symbiotic octocoral species of the Lord Howe Island lagoonal reef bleached. Unbleached Xenia cf crassa colonies had higher Symbiodiniaceae and chlorophyll densities during the marine heatwave compared to other monitoring intervals, while Cladiella sp. 2 densities did not change substantially through time. Previous work on octocoral bleaching has focused primarily on gorgonian octocorals, while this study provides insight into bleaching variability in other octocoral groups. The study also provides further evidence that octocorals may be generally more resistant to bleaching than stony corals in many, but not all, reef ecosystems. Responses to marine heating events vary and should be assessed on a species by species basis.

Coral growth anomalies, neoplasms, and tumors in the Anthropocene.

One of the most widespread coral diseases linked to anthropogenic activities and recorded on reefs worldwide is characterized by anomalous growth formations in stony corals, referred to as coral growth anomalies (GAs). The biological functions of GA tissue include limited reproduction, reduced access to resources, and weakened ability to defend against predators. Transcriptomic analyses have revealed that, in some cases, disease progression can involve host genes related to oncogenesis, suggesting that the GA tissues may be malignant neoplasms such as those developed by vertebrates. The number of studies reporting the presence of GAs in common reef-forming species highlights the urgency of a thorough understanding of the pathology and causative factors of this disease and its parallels to higher organism malignant tissue growth. Here, we review the current state of knowledge on the etiology and holobiont features of GAs in reef-building corals.

Experiment Degree Heating Week (eDHW) as a novel metric to reconcile and validate past and future global coral bleaching studies.

Coral bleaching has increasingly impacted reefs worldwide over the past four decades. Despite almost 40 years of research into the mechanistic, physiological, ecological, biophysical and climatic drivers of coral bleaching, metrics to allow comparison between ecological observations and experimental simulations still do not exist. Here we describe a novel metric - experimental Degree Heating Week (eDHW) - with which to standardise the persistently variable thermal conditions employed across experimental studies of coral bleaching by modify the widely used Degree Heating Week (DHW) metric used in ecological studies to standardise cumulative heat loading.

Rebuilding relationships on coral reefs: Coral bleaching knowledge-sharing to aid adaptation planning for reef users: Bleaching emergence on reefs demonstrates the need to consider reef scale and accessibility when preparing for, and responding to, coral bleaching.

Coral bleaching has impacted reefs worldwide and the predictions of near-annual bleaching from over two decades ago have now been realized. While technology currently provides the means to predict large-scale bleaching, predicting reef-scale and within-reef patterns in real-time for all reef users is limited. In 2020, heat stress across the Great Barrier Reef underpinned the region's third bleaching event in 5 years. Here we review the heterogeneous emergence of bleaching across Heron Island reef habitats and discuss the oceanographic drivers that underpinned variable bleaching emergence. We do so as a case study to highlight how reef end-user groups who engage with coral reefs in different ways require targeted guidance for how, and when, to alter their use of coral reefs in response to bleaching events. Our case study of coral bleaching emergence demonstrates how within-reef scale nowcasting of coral bleaching could aid the development of accessible and equitable bleaching response strategies on coral reefs. Also see the video abstract here: https://youtu.be/N9Tgb8N-vN0.

Promoting inclusive metrics of success and impact to dismantle a discriminatory reward system in science.

Success and impact metrics in science are based on a system that perpetuates sexist and racist "rewards" by prioritizing citations and impact factors. These metrics are flawed and biased against already marginalized groups and fail to accurately capture the breadth of individuals' meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.

Combating ecosystem collapse from the tropics to the Antarctic.

Globally, collapse of ecosystems-potentially irreversible change to ecosystem structure, composition and function-imperils biodiversity, human health and well-being. We examine the current state and recent trajectories of 19 ecosystems, spanning 58° of latitude across 7.7 M km2 , from Australia's coral reefs to terrestrial Antarctica. Pressures from global climate change and regional human impacts, occurring as chronic 'presses' and/or acute 'pulses', drive ecosystem collapse. Ecosystem responses to 5-17 pressures were categorised as four collapse profiles-abrupt, smooth, stepped and fluctuating. The manifestation of widespread ecosystem collapse is a stark warning of the necessity to take action. We present a three-step assessment and management framework (3As Pathway Awareness, Anticipation and Action) to aid strategic and effective mitigation to alleviate further degradation to help secure our future.

Coral bleaching.

Tracy Ainsworth and Barbara Brown introduce the causes and consequences of coral bleaching.

Positive Interactions in the Coral Macro and Microbiome.

Researchers now recognize the importance of the coral microbiome, but they often overlook other species that live on corals and influence coral-microbe interactions. These 'interstitial associates' should be incorporated into the metaorganism concept for insights into how facilitations between associates, corals, and their microbiomes can be leveraged in ecology and restoration.

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

Extreme heat wave events are now causing ecosystem degradation across marine ecosystems. The consequences of this heat-induced damage range from the rapid loss of habitat-forming organisms, through to a reduction in the services that ecosystems support, and ultimately to impacts on human health and society. How we tackle the sudden emergence of ecosystem-wide degradation has not yet been addressed in the context of marine heat waves. An examination of recent marine heat waves from around Australia points to the potential important role that respite or refuge from environmental extremes can play in enabling organismal survival. However, most ecological interventions are being devised with a target of mid to late-century implementation, at which time many of the ecosystems, that the interventions are targeted towards, will have already undergone repeated and widespread heat wave induced degradation. Here, our assessment of the merits of proposed ecological interventions, across a spectrum of approaches, to counter marine environmental extremes, reveals a lack preparedness to counter the effects of extreme conditions on marine ecosystems. The ecological influence of these extremes are projected to continue to impact marine ecosystems in the coming years, long before these interventions can be developed. Our assessment reveals that approaches which are technologically ready and likely to be socially acceptable are locally deployable only, whereas those which are scalable-for example to features as large as major reef systems-are not close to being testable, and are unlikely to obtain social licence for deployment. Knowledge of the environmental timescales for survival of extremes, via respite or refuge, inferred from field observations will help test such intervention tools. The growing frequency of extreme events such as marine heat waves increases the urgency to consider mitigation and intervention tools that support organismal and ecosystem survival in the immediate future, while global climate mitigation and/or intervention are formulated.

A horizon scan of priorities for coastal marine microbiome research.

Research into the microbiomes of natural environments is changing the way ecologists and evolutionary biologists view the importance of microorganisms in ecosystem function. This is particularly relevant in ocean environments, where microorganisms constitute the majority of biomass and control most of the major biogeochemical cycles, including those that regulate Earth's climate. Coastal marine environments provide goods and services that are imperative to human survival and well-being (for example, fisheries and water purification), and emerging evidence indicates that these ecosystem services often depend on complex relationships between communities of microorganisms (the 'microbiome') and the environment or their hosts - termed the 'holobiont'. Understanding of coastal ecosystem function must therefore be framed under the holobiont concept, whereby macroorganisms and their associated microbiomes are considered as a synergistic ecological unit. Here, we evaluate the current state of knowledge on coastal marine microbiome research and identify key questions within this growing research area. Although the list of questions is broad and ambitious, progress in the field is increasing exponentially, and the emergence of large, international collaborative networks and well-executed manipulative experiments are rapidly advancing the field of coastal marine microbiome research.

Characterization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus.

Bacterial diversity associated with corals has been studied extensively, however, localization of bacterial associations within the holobiont is still poorly resolved. Here we provide novel insight into the localization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. In total, 318 and 308 CAMAs were characterized via histological and fluorescent in situ hybridization (FISH) approaches respectively, and shown to be distributed extensively throughout coral tissues collected from five sites in Japan and Australia. The densities of CAMAs within the tissues were negatively correlated with the distance from the coastline (i.e. lowest densities at offshore sites). CAMAs were randomly distributed across the six coral tissue regions investigated. Within each CAMA, bacterial cells had similar morphological characteristics, but bacterial morphologies varied among CAMAs, with at least five distinct types identified. Identifying the location of microorganisms associated with the coral host is a prerequisite for understanding their contributions to fitness. Localization of tissue-specific communities housed within CAMAs is particularly important, as these communities are potentially important contributors to vital metabolic functions of the holobiont.

Rapid Coral Decay Is Associated with Marine Heatwave Mortality Events on Reefs.

Severe marine heatwaves have recently become a common feature of global ocean conditions due to a rapidly changing climate [1, 2]. These increasingly severe thermal conditions are causing an unprecedented increase in the frequency and severity of mortality events in marine ecosystems, including on coral reefs [3]. The degradation of coral reefs will result in the collapse of ecosystem services that sustain over half a billion people globally [4, 5]. Here, we show that marine heatwave events on coral reefs are biologically distinct to how coral bleaching has been understood to date, in that heatwave conditions result in an immediate heat-induced mortality of the coral colony, rapid coral skeletal dissolution, and the loss of the three-dimensional reef structure. During heatwave-induced mortality, the coral skeletons exposed by tissue loss are, within days, encased by a complex biofilm of phototrophic microbes, whose metabolic activity accelerates calcium carbonate dissolution to rates exceeding accretion by healthy corals and far greater than has been documented on reefs under normal seawater conditions. This dissolution reduces the skeletal density and hardness and increases porosity. These results demonstrate that severe-heatwave-induced mortality events should be considered as a distinct biological phenomenon from bleaching events on coral reefs. We also suggest that such heatwave mortality events, and rapid reef decay, will become more frequent as the intensity of marine heatwaves increases and provides further compelling evidence for the need to mitigate climate change and instigate actions to reduce marine heatwaves.

Seeking Resistance in Coral Reef Ecosystems: The Interplay of Biophysical Factors and Bleaching Resistance under a Changing Climate: The Interplay of a Reef's Biophysical Factors Can Mitigate the Coral Bleaching Response.

If we are to ensure the persistence of species in an increasingly warm world, of interest is the identification of drivers that affect the ability of an organism to resist thermal stress. Underpinning any organism's capacity for resistance is a complex interplay between biological and physical factors occurring over multiple scales. Tropical coral reefs are a unique system, in that their function is dependent upon the maintenance of a coral-algal symbiosis that is directly disrupted by increases in water temperature. A number of physical factors have been identified as affecting the biological responses of the coral organism under broadscale thermal anomalies. One such factor is water flow, which is capable of modulating both organismal metabolic functioning and thermal environments. Understanding the physiological and hydrodynamic drivers of organism response to thermal stress improves predictive capabilities and informs targeted management responses, thereby increasing the resilience of reefs into the future.

A place for taxonomic profiling in the study of the coral prokaryotic microbiome.

The enormous variability in richness, abundance and diversity of unknown bacterial organisms inhabiting the coral microbiome have challenged our understanding of their functional contribution to coral health. Identifying the attributes of the healthy meta-organism is paramount for contemporary approaches aiming to manipulate dysbiotic stages of the coral microbiome. This review evaluates the current knowledge on the structure and mechanisms driving bacterial communities in the coral microbiome and discusses two topics requiring further research to define the healthy coral microbiome. (i) We examine the necessity to establish microbial baselines to understand the spatial and temporal dynamics of the healthy coral microbiome and summarise conceptual and logistic challenges to consider in the design of these baselines. (ii) We propose potential mechanical, physical and chemical mechanisms driving bacterial distribution within coral compartments and suggest experiments to test them. Finally, we highlight aspects of the use of 16S amplicon sequencing requiring standardization and discuss its contribution to other multi-omics approaches.

Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere.

Studies of the coral microbiome predominantly characterize the microbial community of the host species as a collective, rather than that of the individual. This ecological perspective on the coral microbiome has led to the conclusion that the coral holobiont is the most diverse microbial biosphere studied thus far. However, investigating the microbiome of the individual, rather than that of the species, highlights common and conserved community attributes which can provide insights into the significance of microbial associations to the host. Here, we show there are consistent characteristics between individuals in the proposed three components of the coral microbiome (i.e., "environmentally responsive community," "resident or individual microbiome," and "core microbiome"). We found that the resident microbiome of a photoendosymbiotic coral harbored <3% (∼605 phylotypes) of the 16S rRNA phylotypes associated with all investigated individuals of that species ("species-specific microbiome") (∼21,654 phylotypes; individuals from Pachyseris speciosa [n = 123], Mycedium elephantotus [n = 95], and Acropora aculeus [n = 91] from 10 reef locations). The remaining bacterial phylotypes (>96%) (environmentally responsive community) of the species-specific microbiome were in fact not found in association with the majority of individuals of the species. Only 0.1% (∼21 phylotypes) of the species-specific microbiome of each species was shared among all individuals of the species (core microbiome), equating to ∼3.4% of the resident microbiome. We found taxonomic redundancy and consistent patterns of composition, structure, and taxonomic breadth across individual microbiomes from the three coral species. Our results demonstrate that the coral microbiome is structured at the individual level.IMPORTANCE We propose that the coral holobiont should be conceptualized as a diverse transient microbial community that is responsive to the surrounding environment and encompasses a simple, redundant, resident microbiome and a small conserved core microbiome. Most importantly, we show that the coral microbiome is comparable to the microbiomes of other organisms studied thus far. Accurately characterizing the coral-microbe interactions provides an important baseline from which the functional roles and the functional niches within which microbes reside can be deciphered.