Posts Tagged 'porifera'

Deep-sea sponges in an Anthropocene ocean

Sponges (Porifera) are among the oldest multicellular animals on planet earth and are abundant throughout all oceans. From shallow, warm waters to the dark, cold deep sea. Sponges move large quantities of seawater through their body while efficiently removing dissolved and particulate nutrients. Their large filter capacity makes them important links in marine food webs as they are able to access nutrient sources that are unavailable to the majority of marine fauna and channel this energy to higher trophic levels. In the North Atlantic Ocean (NAO) sponges form dense aggregations, so called sponge rounds, that provide ecosystem services such as habitat provision, nutrient cycling and provision of novel, bioactive compounds. It remains unclear whether these deep-sea sponge grounds can continue to provide these services in a changing ocean that is increasingly industrialized. The physicochemical properties of the North Atlantic Ocean will be altered by human induced climate change. The aim of this thesis is to address this knowledge gaps by quantifying the basic eco-physiological processes such as oxygen consumption, clearance rate and uptake/release of inorganic nutrients of two habitat forming deep-sea sponges under the cumulative impacts of warmer, acidified seawater and the exposure to different types of re-suspended particles. The research underlying this thesis was part of the EU-funded research project Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation (SponGES). Two model deep sea sponge species were used, Geodia barretti and Vazella pourtalesi. G. barretti collected from 300 m water depth in the Barents Sea, were exposed to four treatments resembling future ocean conditions (no treatment, 4 °C increase in seawater temperature, decrease of seawater pH by 0.3, and a combination of the high temperature, low pH). Over the course of 39 weeks, oxygen consumption, dissolved inorganic nutrient fluxes, and bacterioplankton clearance rates were measured as indicators of metabolic activity. All indicators within each sponge individual and per treatment were highly variable over time, and no effect of manipulated seawater treatments on these parameters could be demonstrated. Oxygen consumption rates in all groups closely followed a seasonal pattern, potentially caused by (a)biotic cues in the natural seawater flowing through the experimental aquaria. While similar metabolic rates across all treatments suggest that G. barretti physiologically coped with simulated future ocean conditions, tissue necrosis that developed in experimental animals might indicate that the response of the complex, high microbial G. barretti sponge (i.e., sponge host and microbial symbionts) to future ocean conditions may not be reflected in basic physiological processes. In addition to large scale changes of ocean conditions, also bottom trawling activities interact with the dense sponge aggregations. Bottom trawling has been identified as the most severe direct industrial threat to abundant sponge grounds by removing sponge biomass and indirect by re-suspending bottom sediments. Plumes of re-suspended sediment potentially smother and clog the aquiferous system of filter-feeding sponges with unknown implications for their health. The physiological responses of repeated exposure to natural sediment were studied in the glass sponge Vazella pourtalesii, which forms dense sponge grounds in Emerald Basin off Nova Scotia, Canada. Ex situ chamber-based measurements of bacterial clearance and oxygen consumption (respiration) rates indicated that the animals were able to cope with elevated concentrations of suspended sediment, as they expressed normal clearance and respiration rates over 7 days of sediment exposure. However, clearance rates significantly declined after 14 days of sediment exposure and the animals visibly accumulated sediment in their tissue. Therefore, long-term exposure to elevated concentrations of suspended sediment should be avoided in order to minimize adverse effects on the abundant Vazella sponge grounds. While sponges seem to cope with environmental changes and limited exposure to suspended particles as occurs in their natural environment, the response to cumulative stressors indicated impaired health. Exposure to a field relevant concentration of suspended sediment (50 mg L-1) and future ocean conditions (pH decrease of 0.2 units, temperature increase of 3 °C) on the physiological performance of Geodia barretti resulted in a cessation of pumping. Oxygen consumption rates remained unchanged under low pH and high temperature treatments and indicate mechanisms of pumping-independent mass transfer of oxygen. A small, but statistically significant shift in the microbiome associated with G. barretti was observed and possibly related to coping with cumulative stressors in this deep-sea sponge species. The synergistic nature of the treatment-specific effects has the potential to adversely affect the physiological fitness of this dominating sponge species in the North Atlantic Ocean. In addition to deep-sea fisheries the nascent industry of subsea mining is prospecting abundant mineral resources present in the deep sea. The extraction of subsea minerals, such as seafloor massive sulphide (SMS) deposits, will expose adjacent marine ecosystems to suspended particle plumes charged with elevated concentrations of heavy metals and other potentially toxic compounds. Up to date there is no information about the impact of mining activities on deep-sea benthic ecosystems such as abundant deep-sea sponge grounds in the North Atlantic Ocean. To simulate the effects of mining plumes on benthic life in the deep-sea, Geodia barretti and an associated brittle star genus were exposed to a field-relevant concentration of 30 mg L-1 suspended particles of crushed SMS deposits. Three weeks of exposure to suspended particles of crushed SMS resulted in a tenfold higher rate of tissue necrosis in sponges. All brittle stars in the experiment already perished within ten days of exposure. SMS particles were evidently accumulated in the sponge’s mesohyl and concentrations of iron and copper were 10 times elevated in SMS exposed individuals. Oxygen consumption and clearance rates were significantly retarded after the exposure to SMS particles, hampering the physiological performance of G. barretti. These adverse effects of crushed SMS deposits on G. barretti and its associated brittle star species potentially cascade in disruptions of benthic-pelagic coupling processes in the deep sea. More elaborate studies are advisable to identify threshold levels, management concepts and mitigation measures to minimize the impact of deep-sea mining plumes on benthic life. Sponges were shown to express high coping capacities towards fluctuations of environmental parameters within their habitat. However, additional stressors or persistence of sub-optimal conditions over extended time scales can challenge sponge’s ability to endure cumulative effects. Given the ecosystem services sponge grounds in the North Atlantic Ocean provide, industrial operations should ascertain refuges for deep-sea sponges faced with global ocean changes.

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The influences of diurnal variability and ocean acidification on the bioerosion rates of two reef-dwelling Caribbean sponges

Ocean acidification (OA) is expected to modify the structure and function of coral reef ecosystems by reducing calcification, increasing bioerosion, and altering the physiology of many marine organisms. Much of our understanding of these relationships is based upon experiments with static OA treatments, though evidence suggests that the magnitude of diurnal fluctuations in carbonate chemistry may modulate the calcification response to OA. These light-mediated swings in seawater pH are projected to become more extreme with OA, yet their impact on bioerosion remains unknown. We evaluated the influence of diurnal carbonate chemistry variability on the bioerosion rates of two Caribbean sponges: the zooxanthellate Cliona varians and azooxanthellate Cliothosa delitrix. Replicate fragments from multiple colonies of each species were exposed to four precisely-controlled pH treatments: contemporary static (8.05 ± 0.00; mean pH ± diurnal pH oscillation), contemporary variable (8.05 ± 0.10), future OA static (7.80 ± 0.00), and future OA variable (7.80 ± 0.10). Significantly enhanced bioerosion rates, determined using buoyant weight measurements, were observed under more variable conditions in both the contemporary and future OA scenarios for C. varians, whereas the same effect was only apparent under contemporary pH conditions for C. delitrix. These results indicate that variable carbonate chemistry has a stimulating influence on sponge bioerosion, and we hypothesize that bioerosion rates evolve non-linearly as a function of pCO2 resulting in different magnitudes and directions of rate enhancement/reduction between day and night, even with an equal fluctuation around the mean. This response appeared to be intensified by photosymbionts, evident by the consistently higher percent increase in bioerosion rates for photosynthetic C. varians across all treatments. These findings further suggest that more variable natural ecosystems may presently experience elevated sponge bioerosion rates and that the heightened impact of OA enhanced bioerosion on reef habitat could occur sooner than prior predictions.

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The impact of carbonate chemistry on bioeroding sponges and the persistence of south Florida coral reefs

Coral reef ecosystems are being threatened by the growing effects of anthropogenically-induced climate change. At a global-scale, diminished reef development and growth potential has culminated in a consequential shift towards the net loss of reef habitat. While the impacts of climate change have been well established for reef calcifiers, the response by bioeroders is vastly understudied in the literature.      

This Ph.D project evaluated the impacts of ocean acidification (OA) and diurnal carbonate chemistry variability on zooxanthellate (C. varians) and azooxanthellate (P. lampa and C. delitrix) sponge species common to Caribbean reef ecosystems. Physiological and molecular analysis identified a sponge stress response under OA conditions, as depressed bioerosion rates and differentially expressed genes implicated in a generalized stress response were measured in the 7.75 pH treatment. Diurnal carbonate chemistry variability was also found to be a significant driver of sponge bioerosion, with higher bioerosion rates measured under both contemporary and OA variable conditions relative to that of the static treatment groups, an effect that was more pronounced for the zooxanthellate sponge species.      

Additionally, this Ph.D project used a carbonate budget approach to evaluate spatial and temporal trends in reef growth potential for 723 South Florida reef sites. The results reported a net erosional state for coral reefs throughout the Florida Reef Tract (FRT). While these data detailed a considerable trend towards habitat loss throughout South Florida, the inclusion of reef type data revealed that mid-channel reefs in the Upper and Lower Keys may be potential hold-outs for reef development compared to their inshore and offshore counterparts.      

Altogether, the conclusions drawn from these studies address critical research gaps related to sponge bioerosion and reef development. This Ph.D will enhance prospective evaluations of habitat growth potential and improve future assessments modeling the fate of coral reef ecosystems in response to projected environmental scenarios.

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Impact of lowered pH on the morphological, physiological, and microbial community composition of the temperate calcareous sponge, Grantia sp.

Global atmospheric carbon dioxide (CO₂) concentrations have been increasing at unprecedented rates since the industrial revolution. The ocean has been acting as a buffer, absorbing CO₂, resulting in rising sea temperature (ocean warming; OW) and lowering its pH (ocean acidification; OA). OA is known to cause reductions in the calcification rates of marine calcifiers, resulting in dissolution of calcium carbonate shells and skeletons. Sponges have important functional and structural roles in marine ecosystems and there is some evidence to suggest that sponges may be “winners” under future ocean climate conditions due to their high level of resilience to OA and OW and the increased availability of space as a result of reductions in more sensitive calcifying species. Although this may be the case for those sponges with skeletons made up of siliceous spicules, little is known about how calcareous sponges, with calcite spicules, may react to OA conditions. This thesis addresses a knowledge gap on how temperate calcareous sponges may respond to OA using Grantia sp. as a model species. A twenty-eight-day experiment with three control (pH 8.0) tanks and three OA (based on IPCC (RCP8.5); pH 7.6) tanks was used to measure changes in sponge size, spicule size, spicule deformation, respiration rate and microbial community structure. I found no signs of corrosion or significant change in area of sponges, however, there was a significant 25% reduction in the spicule size under the projected climate change OA “worst case scenario” conditions, a sign that sponge growth was impacted under stressful external pressure. How this reduction is spicule size will impact the sponge is still unknown. Respiration rates of sponges were not significantly different between the control or treatment sponges, and the microbiome of control and OA sponges did not significantly differ, but they did change significantly over time (T0 compared to T28 (final day of the experiment). The microbiome over time changed with increasing abundance of microbes known to have a role in nutrient cycling and assisting in marine host’s acclimation to new niches with varied environmental conditions. My results suggest that while the physiology of Grantia sp. is not significantly affected by low pH conditions consistent with those predicted for 2100 under worst case climate scenarios, spicules were impacted with treatment sponges having smaller spicules. The consequences and mechanisms resulting in smaller spicules need further investigation. Overall, this study provides evidence that like many demosponges, calcareous sponges may have some resilience to OA impacts.

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Phototrophic sponge productivity may not be enhanced in a high CO2 world

Sponges are major components of benthic communities across the world and have been identified as potential “winners” on coral reefs in the face of global climate change as result of their tolerance to ocean warming and acidification (OA). Previous studies have also hypothesised that photosymbiont-containing sponges might have higher productivity under future OA conditions as a result of photosymbionts having increased access to CO2 and subsequently greater carbon production. Here we test this hypothesis for a widespread and abundant photosymbiont-containing sponge species Lamellodysidea herbacea at a CO2 seep in Papua New Guinea simulating OA conditions. We found seep sponges had relatively higher cyanobacterial abundance, chlorophyll concentrations and symbiont photosynthetic efficiency than non-seep sponges, and a three-fold higher sponge abundance at the seep site. However, while gross oxygen production was the same for seep and non-seep sponges, seep sponge dark respiration rates were higher and instantaneous photosynthesis: respiration (P:R) ratios were lower. We show that while photosymbiont containing sponges may not have increased productivity under OA, they are able to show flexibility in their relationships with microbes and offset increased metabolic costs associated with climate change associated stress.

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Understanding the impacts of environment and parasitism on Eastern oyster (Crassostrea virginica) vulnerability to ocean acidification

The global process of ocean acidification caused by the absorption of increased atmospheric carbon dioxide decreases the concentration of carbonate ions and reduces the associated seawater saturation state (ΩCaCO3) – making it more energetically costly for marine calcifying organisms to build their shells or skeletons. Bivalves are particularly vulnerable to the adverse effects of ocean acidification on calcification, and they inhabit estuaries and coastal zones – regions most susceptible to ocean acidification. However, the response of an individual to elevated pCO2 can depend on the carbonate chemistry dynamics of its current environment and the environment of its parents. Additionally, an organism’s response to ocean acidification can depend on its ability to control the chemistry at the site of calcification. Biotic and abiotic stressors can modify bivalves’ control of calcifying fluid chemistry – known as extrapallial fluid (EPF). Understanding the responses of bivalves – which are foundation species – to ocean acidification is essential for predicting the impacts of oceanic change on marine communities. This dissertation uses a culturally, ecologically, and economically important bivalve in the northwest Atlantic – the Eastern oyster (Crassostrea virginica) – to explore the effects of environment and species interactions on responses to elevated pCO2.

Chapter 2 describes a field study that characterized diurnal and seasonal carbonate chemistry dynamics of two estuaries in the Gulf of Maine that support Eastern oyster populations. The estuaries were monitored at high temporal resolution (half-hourly) over four years (2018-2021) using pH and conductivity loggers. Measured pH, salinity, and temperature were used to calculate carbonate chemistry parameters. Both estuaries exhibited strong seasonal and diurnal fluctuations in carbonate chemistry. They also experienced pCO2 values that greatly exceeded current atmospheric carbon dioxide levels and those projected for the year 2100.

Chapter 3 describes a laboratory experiment that examined the capacity of intergenerational exposure to mitigate the adverse effects of ocean acidification on larval growth, shell morphology, and survival. Adult oysters were cultured in control or elevated pCO2 conditions for 30 days then crossed using a North Carolina II cross design. Larvae were grown for three days under control and elevated pCO2 conditions. Intergenerational exposure to elevated pCO2 conditions benefited early larval growth and shell morphology, but not survival. However, parental exposure was insufficient to completely counteract the adverse effects of the elevated pCO2 treatment on shell formation and survival.

Chapter 4 describes a laboratory experiment that examined the interplay between ocean acidification and parasite-host dynamics. Eastern oysters infested and not infested with bioeroding sponge (Cliona sp.) were cultured under three pCO2 conditions (539, 1040, 3294 ppm) and two temperatures (23, 27˚C) for 70 days to assess oyster control of EPF chemistry, growth, and survival. Bioeroding sponge infestation and elevated pCO2 reduced oyster net calcification and EPF pH but did not affect condition or survival. Infested oyster EPF pH was consistently lower than seawater pH, while EPF dissolved inorganic carbon was consistently elevated relative to seawater. These findings suggested that infested oysters effectively precipitated repair shell to prevent seawater intrusion into extrapallial fluid through bore holes across all treatments.

Chapter 5 characterizes the concentration of a suite of 56 elements normalized to calcium in EPF and shell of Crassostrea virginica grown under three pCO2 conditions (570, 990, 2912 ppm) and sampled at four timepoints (days 2, 9, 79, 101) to assess effects of pCO2 on organismal control of EPF and shell elemental composition and EPF-to-shell elemental partitioning. Elevated pCO2 significantly influenced the relative abundance of elements in the EPF (29) and shell (13) and altered EPF-to-shell elemental partitioning for 45 elements. Importantly, elevated pCO2 significantly influenced the concentration of several elements in C. virginica shell that are used in other biogenic carbonates as paleo-proxies for other environmental parameters. This result suggests that elevated pCO2 could influence the accuracy of paleo reconstructions.

Overall, this dissertation provides insights that can help improve our understanding of past, present, and future ocean environments. Understanding current local carbonate chemistry dynamics and the capacity for C. virginica to acclimate intergenerationally to elevated pCO2 can inform site and stock selection for aquaculture and restoration efforts. Studying parasite-host environment interactions provides critical insights into the potential for parasitism to alter responses to future ocean acidification. Finally, exploring the impact of elevated pCO2 on elemental composition of EPF and shell allowed us to understand better biomineralization processes, identify potential proxies for seawater pCO2 in bivalves, and offer insights that could help improve the accuracy of paleo reconstructions.

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Comparative transcriptomics reveals altered species interaction between the bioeroding sponge Cliona varians and the coral Porites furcata under ocean acidification

Bioeroding sponges interact and compete with corals on tropical reefs. Experimental studies have shown global change alters this biotic interaction, often in favor of the sponge. Ocean acidification in particular increases sponge bioerosion and reduces coral calcification, yet little is known about the molecular basis of these changes. We used RNA-Seq data to understand how acidification impacts the interaction between the bioeroding sponge, Cliona varians, and the coral, Porites furcata, at the transcriptomic level. Replicate sponge and coral genets were exposed to ambient (8.1 pH) and acidified (7.6 pH) conditions in isolation and in treatments where they were joined for 48hrs. The coral had a small gene expression response (tens of transcripts) to the sponge, suggesting it does little at the transcriptomic level to deter sponge overgrowth. By contrast, the sponge differentially expressed 7320 transcripts in response to the coral under ambient conditions and 3707 transcripts in response to acidification. Overlap in the responses to acidification and the coral, 2500 transcripts expressed under both treatments, suggests a similar physiological response to both cues. The sponge expressed 50x fewer transcripts in response to the coral under acidification, suggesting energetic costs of bioerosion, and other cellular processes, are lower for sponges under acidification. Our results suggest how acidification drives ecosystem-level changes in the accretion/bioerosion balance on coral reefs. This shift is not only the result of changes to the thermodynamic balance of these chemical reactions but also the result of active physiological responses of organisms to each other and their abiotic environment.

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Biomineralization: integrating mechanism and evolutionary history

Calcium carbonate (CaCO3) biomineralizing organisms have played major roles in the history of life and the global carbon cycle during the past 541 Ma. Both marine diversification and mass extinctions reflect physiological responses to environmental changes through time. An integrated understanding of carbonate biomineralization is necessary to illuminate this evolutionary record and to understand how modern organisms will respond to 21st century global change. Biomineralization evolved independently but convergently across phyla, suggesting a unity of mechanism that transcends biological differences. In this review, we combine CaCO3 skeleton formation mechanisms with constraints from evolutionary history, omics, and a meta-analysis of isotopic data to develop a plausible model for CaCO3 biomineralization applicable to all phyla. The model provides a framework for understanding the environmental sensitivity of marine calcifiers, past mass extinctions, and resilience in 21st century acidifying oceans. Thus, it frames questions about the past, present, and future of CaCO3 biomineralizing organisms.

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Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification


Although climate change is expected to decimate coral reefs, the combined impacts of ocean-warming and acidification on coral reef biodiversity remains largely unmeasured. Here, we present a two-year mesocosm experiment to simulate future ocean acidification and ocean-warming to quantify the impacts on species richness, community composition, and community structure. We find that species richness is equivalent between the dual-stressor and present-day treatments but that the community shuffles, undoubtedly altering ecosystem function. However, our ability to predict the outcomes of such community shuffling remains limited due to the critical knowledge gap regarding ecological functions, life histories, and distributions for most members of the cryptobenthic community that account for the majority of the biodiversity within these iconic ecosystems.


Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (−0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity–function relationships and ecosystem responses to future climate conditions.

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DNA metabarcoding to examine the biodiversity of coral reef cryptobiota

Coral reefs are among the most biologically diverse, complex, and productive of ecosystems. The vast majority of coral reef biodiversity is made up of the small and cryptic organisms living unseen by most within the reef matrix. This hidden community, the cryptobiota, are a critical component of coral reef trophic dynamics and play an essential role in nutrient recycling that enable reefs to thrive in oligotrophic environments. Despite their ecological importance, the cryptobiota are often ignored because they live deep within the reef matrix and require significant taxonomic expertise and time to collect and identify. As a result, our perceptions of coral reef biodiversity across marine gradients and how it will respond to climatic change is based on observable surface-dwelling taxa, such as corals and fish. Using DNA metabarcoding technology, this research fills an extensive knowledge gap about the diversity and distribution of the important and understudied coral reef cryptobiota community. The objectives of this dissertation were to (i) evaluate metabarcoding performance on marine sponges, a prominent and ecologically vital member of the cryptobenthos that is one of the most difficult metazoans to identify to species using both taxonomic and molecular methods; (ii) investigate the individual and combined effects of ocean warming and acidification on cryptobiota biodiversity; and (iii) examine cryptobiota diversity along the most striking macrospatial diversity gradient in the marine tropics. Contrary to expectations, this research (i) demonstrated that the metabarcoding approach performs much better than expected in capturing sponge richness; (ii) discovered that diversity shuffles but does not decline under the combined stressors of ocean warming and acidification; and (iii) cryptobiotic diversity undermines the tropical Pacific longitudinal diversity gradient defined by corals and fish. These results contribute towards reshaping the way we consider coral reef biodiversity under different oceanographic, geographic and climatic regimes.

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The effect of global warming and ocean acidification on Halichondira panicea bacteria

Marine sponges are becoming an increasing source of novel biomedical and antibacterial compounds. Many of these compounds are synthesized as secondary metabolites from symbiotic bacteria and have immense potential in the pharmaceutical industry. However, climate change may pose a threat to the viability of marine sponges and result in the loss of future medical discoveries. Therefore, this paper looks at the effect climate change may have on marine sponges by subjecting fragments of the marine sponge, Halichondria panicea, into aquaria representing different climate change scenarios to study the effect that global warming and ocean acidification may have on its symbiotic bacteria. To model climate change towards the end of the 21st century, conditions from the IPCC’s 2014 climate change report were simulated to determine specific growth conditions. The fragments were placed in the different RCP growth conditions for two weeks, then dissociated, filtered, and the extracts incubated on Hektoen enteric agar for 48 hours. The results showed that climate change has adverse effects on the marine sponge, Halichondria panicea, by decreasing their symbiotic bacterial population by around 18 %

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Microbiome diversity and host immune functions influence survivorship of sponge holobionts under future ocean conditions

The sponge-associated microbial community contributes to the overall health and adaptive capacity of the sponge holobiont. This community is regulated by the environment and the immune system of the host. However, little is known about the effect of environmental stress on the regulation of host immune functions and how this may, in turn, affect sponge–microbe interactions. In this study, we compared the bacterial diversity and immune repertoire of the demosponge, Neopetrosia compacta, and the calcareous sponge, Leucetta chagosensis, under varying levels of acidification and warming stress based on climate scenarios predicted for 2100. Neopetrosia compacta harbors a diverse microbial community and possesses a rich repertoire of scavenger receptors while L. chagosensis has a less diverse microbiome and an expanded range of pattern recognition receptors and immune response-related genes. Upon exposure to RCP 8.5 conditions, the microbiome composition and host transcriptome of N. compacta remained stable, which correlated with high survival (75%). In contrast, tissue necrosis and low survival (25%) of L. chagosensis was accompanied by microbial community shifts and downregulation of host immune-related pathways. Meta-analysis of microbiome diversity and immunological repertoire across poriferan classes further highlights the importance of host–microbe interactions in predicting the fate of sponges under future ocean conditions.

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Ocean acidification and direct interactions affect coral, macroalga, and sponge growth in the Florida Keys

Coral reef community composition, function, and resilience have been altered by natural and anthropogenic stressors. Future anthropogenic ocean and coastal acidification (together termed “acidification”) may exacerbate this reef degradation. Accurately predicting reef resilience requires an understanding of not only direct impacts of acidification on marine organisms but also indirect effects on species interactions that influence community composition and reef ecosystem functions. In this 28-day experiment, we assessed the effect of acidification on coral–algal, coral–sponge, and algal–sponge interactions. We quantified growth of corals (Siderastrea radians), fleshy macroalgae (Dictyota spp.), and sponges (Pione lampa) that were exposed to local summer ambient (603 μatm) or elevated (1105 μatm) pCO2 seawater. These species are common to hard-bottom communities, including shallow reefs, in the Florida Keys. Each individual was maintained in isolation or paired with another organism. Coral growth (net calcification) was similar across seawater pCO2 and interaction treatments. Fleshy macroalgae had increased biomass when paired with a sponge but lost biomass when growing in isolation or paired with coral. Sponges grew more volumetrically in the elevated seawater pCO2 treatment (i.e., under acidification conditions). Although these results are limited in temporal and spatial scales due to the experimental design, they do lend support to the hypothesis that acidification may facilitate a shift towards increased sponge and macroalgae abundance by directly benefiting sponge growth which in turn may provide more dissolved inorganic nitrogen to macroalgae in the Florida Keys.

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Microbiome diversity and host immune functions may define the fate of sponge holobionts under future ocean conditions

The sponge-associated microbial community contributes to the overall health and adaptive capacity of the sponge holobiont. This community is regulated by the environment, as well as the immune system of the host. However, little is known about the effect of environmental stress on the regulation of host immune functions and how this may, in turn, affect sponge-microbe interactions. In this study, we compared the microbiomes and immune repertoire of two sponge species, the demosponge, Neopetrosia compacta and the calcareous sponge, Leucetta chagosensis, under varying levels of acidification and warming stress. Neopetrosia compacta harbors a diverse bacterial assemblage and possesses a rich repertoire of scavenger receptors while L. chagosensis has a less diverse microbiome and an expanded range of pattern recognition receptors and proteins with immunological domains. Upon exposure to warming and acidification, the microbiome and host transcriptome of N. compacta remained stable, which correlated with high survival. In contrast, the bacterial community of L. chagosensis exhibited drastic restructuring and widespread downregulation of host immune-related pathways, which accompanied tissue necrosis and mortality. Differences in microbiome diversity and immunological repertoire of diverse sponge groups highlight the central role of host-microbe interactions in predicting the fate of sponges under future ocean conditions.

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Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau

Ocean warming and acidification caused by the increase of atmospheric carbon dioxide are now thought to be major threats to coral reefs on a global scale. Here we evaluated the environmental conditions and benthic community structures in semi-closed Nikko Bay at the inner reef area in Palau, which has high p CO 2 and seawater temperature conditions with high zooxanthellate coral coverage. This bay is a highly sheltered system with organisms showing low connectivity with surrounding environments, making this bay a unique site for evaluating adaptation and acclimatization responses of organisms to warmed and acidified environments. Seawater p CO 2 /Ω arag showed strong graduation ranging from 380 to 982 µatm (Ω arag : 1.79-3.66) and benthic coverage, including soft corals and turf algae, changed along with Ω arag while hard coral coverage did not. In contrast to previous studies, net calcification was maintained in Nikko Bay even under very low mean Ω arag (2.44). Reciprocal transplantation of the dominant coral Porites cylindrica showed that the calcification rate of corals from Nikko Bay did not change when transplanted to a reference site, while calcification of reference site corals decreased when transplanted to Nikko Bay. Corals transplanted out of their origin sites also showed the highest interactive respiration (R) and lower photosynthesis (P) to respiration (P:R). The results of this study give important insights about the potential local acclimatization and adaptation capacity of corals to different environmental conditions including p CO 2 and temperature.

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Cross‐generational effects of climate change on the microbiome of a photosynthetic sponge

Coral reefs are facing increasing pressure from rising seawater temperatures and ocean acidification. Sponges have been proposed as possible winners in the face of climate change; however, little is known about the mechanisms underpinning their predicted tolerance. Here we assessed whether microbiome‐mediated cross‐generational acclimatization could enable the photosynthetic sponge Carteriospongia foliascens to survive under future climate scenarios. To achieve this, we first established the potential for vertical (cross‐generational) transmission of symbionts. Sixty‐four amplicon sequence variants accounting for >90% of the total C. foliascens microbial community were present across adult, larval and juvenile life stages, showing that a large proportion of the microbiome is vertically acquired and maintained. When C. foliascens were exposed to climate scenarios projected for 2050 and 2100, the host remained visibly unaffected (i.e. no necrosis/bleaching) and the overall microbiome was not significantly different amongst treatments in adult tissue, the respective larvae or recruits transplanted amongst climate treatments. However, indicator species analysis revealed that parental exposure to future climate scenarios altered the presence and abundance of a small suite of microbial taxa in the recruits, thereby revealing the potential for microbiome‐mediated cross‐generational acclimatization through both symbiont shuffling and symbiont switching within a vertically acquired microbiome.

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Warming and acidification threaten glass sponge Aphrocallistes vastus pumping and reef formation

The glass sponge Aphrocallistes vastus contributes to the formation of large reefs unique to the Northeast Pacific Ocean. These habitats have tremendous filtration capacity that facilitates flow of carbon between trophic levels. Their sensitivity and resilience to climate change, and thus persistence in the Anthropocene, is unknown. Here we show that ocean acidification and warming, alone and in combination have significant adverse effects on pumping capacity, contribute to irreversible tissue withdrawal, and weaken skeletal strength and stiffness of A. vastus. Within one month sponges exposed to warming (including combined treatment) ceased pumping (50–60%) and exhibited tissue withdrawal (10–25%). Thermal and acidification stress significantly reduced skeletal stiffness, and warming weakened it, potentially curtailing reef formation. Environmental data suggests conditions causing irreversible damage are possible in the field at +0.5 °C above current conditions, indicating that ongoing climate change is a serious and immediate threat to A. vastus, reef dependent communities, and potentially other glass sponges.

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A high biodiversity mitigates the impact of ocean acidification on hard-bottom ecosystems

Biodiversity loss and climate change simultaneously threaten marine ecosystems, yet their interactions remain largely unknown. Ocean acidification severely affects a wide variety of marine organisms and recent studies have predicted major impacts at the pH conditions expected for 2100. However, despite the renowned interdependence between biodiversity and ecosystem functioning, the hypothesis that the species’ response to ocean acidification could differ based on the biodiversity of the natural multispecies assemblages in which they live remains untested. Here, using experimentally controlled conditions, we investigated the impact of acidification on key habitat-forming organisms (including corals, sponges and macroalgae) and associated microbes in hard-bottom assemblages characterised by different biodiversity levels. Our results indicate that, at higher biodiversity, the impact of acidification on otherwise highly vulnerable key organisms can be reduced by 50 to >90%, depending on the species. Here we show that such a positive effect of a higher biodiversity can be associated with higher availability of food resources and healthy microbe-host associations, overall increasing host resistance to acidification, while contrasting harmful outbreaks of opportunistic microbes. Given the climate change scenarios predicted for the future, we conclude that biodiversity conservation of hard-bottom ecosystems is fundamental also for mitigating the impacts of ocean acidification.

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Changes in the metabolic potential of the sponge microbiome under ocean acidification

Anthropogenic CO2 emissions are causing ocean acidification, which can affect the physiology of marine organisms. Here we assess the possible effects of ocean acidification on the metabolic potential of sponge symbionts, inferred by metagenomic analyses of the microbiomes of two sponge species sampled at a shallow volcanic CO2 seep and a nearby control reef. When comparing microbial functions between the seep and control sites, the microbiome of the sponge Stylissa flabelliformis (which is more abundant at the control site) exhibits at the seep reduced potential for uptake of exogenous carbohydrates and amino acids, and for degradation of host-derived creatine, creatinine and taurine. The microbiome of Coelocarteria singaporensis (which is more abundant at the seep) exhibits reduced potential for carbohydrate import at the seep, but greater capacity for archaeal carbon fixation via the 3-hydroxypropionate/4-hydroxybutyrate pathway, as well as archaeal and bacterial urea production and ammonia assimilation from arginine and creatine catabolism. Together these metabolic features might contribute to enhanced tolerance of the sponge symbionts, and possibly their host, to ocean acidification.

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So long and thanks for all the sponge: cryptic intertidal communities, consequences of ocean acidification, and new directions for science education

Ocean acidification (OA), defined as the reduction in the pH of global oceans, is predicted to have negative impacts on marine invertebrates. Within the past two decades there have been hundreds of studies on the effects of OA on the fitness, survival, and growth of many marine organisms, and yet there are several large gaps in our understanding. Many OA studies focus on one population (e.g. only sample from one site/location) of a widespread species and then make generalizations about that species as a whole. This is problematic for species that are spread between habitats with different levels of acidification. My work in Chapters 3 and 4 addresses the response of multiple populations of an important intertidal invertebrate to ocean acidification conditions on the Oregon coast; I describe the impacts of OA on the early life history (Chapter 3) and adult physiology (Chapter 4) of the common breadcrumb sponge Halichondria panicea. To investigate if H. panicea are adapted to local conditions, I utilized the persistent pattern of acidification that exists on the cape scale along the Oregon coast. I compared the responses of sponge populations that persist in areas of high, intermediate, and low acidification. I used both field and laboratory experiments to investigate the potential for local adaptation or acclimatization to OA conditions in H. panicea. In Chapter 3 I found that sponge larvae from areas that experience persistently high levels of ocean acidification may be less resilient to future levels of OA vs. larvae from other less acidified regions. Negative carryover effects for early exposure during brooding may result in increased larval mortality and faster rates of settlement; there were no effects of treatment on post-settlement processes for either population. Chapter 3 highlights a novel response of sponges to OA and reveals a potential population bottleneck during the critical larval stage for pre-exposed sponges under future OA conditions. Chapter 4 builds on the work of Chapter 3 by examining the response of adult sponges from high, middle, and low areas of OA along the Oregon coast. I used a common garden approach to untangle the effects of environmental acclimation and adaptation in a reciprocal transplant and mesocosm experiment. I observed changes in survival, mass, and Chlorophyll a (Chl- a) concentration. Consistent with Chapter 3, I found that prior exposure to OA resulted in increased mortality during the transplant and mesocosm experiment, although we found no evidence of treatment- or population-dependent effects on mass and chlorophyll a concentration in H. panicea populations. Combined, results of Chapters 3 and 4 suggests that sponges from highly acidified regions may be living near a threshold, past which the fitness of both larvae and adults would be compromised, with implications for the population as a whole.

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