Breakdown Of Symbiosis Research Articles

Should I stay or should I go? Coral bleaching from the symbionts' perspective.

Coral bleaching, the stress-induced breakdown of coral-algal symbiosis, threatens reefs globally. Paradoxically, despite adverse fitness effects, corals bleach annually, even outside of abnormal temperatures. This generally occurs shortly after the once-per-year mass coral spawning. Here, we propose a hypothesis linking annual coral bleaching and the transmission of symbionts to the next generation of coral hosts. We developed a dynamic model with two symbiont growth strategies, and found that high sexual recruitment and low adult coral survivorship and growth favour bleaching susceptibility, while the reverse promotes bleaching resilience. Otherwise, unexplained trends in the Indo-Pacific align with our hypothesis, where reefs and coral taxa exhibiting higher recruitment are more bleaching susceptible. The results from our model caution against interpreting potential shifts towards more bleaching-resistant symbionts as evidence of climate adaptation-we predict such a shift could also occur in declining systems experiencing low recruitment rates, a common scenario on today's reefs.

Coevolution and dependency influence resistance of mutualists to exploitation

A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown.

Comparative physiology reveals heat stress disrupts acid-base homeostasis independent of symbiotic state in the model cnidarian Exaiptasia diaphana.

Climate change threatens the survival of symbiotic cnidarians by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct versus indirect heat effects on the host, as it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C and +6°C) for 15-18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid-base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate.

The highly developed symbiotic system between the solar-powered nudibranch Pteraeolidia semperi and Symbiodiniacean algae

The intricate coexistence of Symbiodiniacean algae with a diverse range of marine invertebrates underpins the flourishing biodiversity observed within coral reef ecosystems. However, the breakdown of Symbiodiniaceae-host symbiosis endangers these ecosystems, necessitating urgent study of the symbiotic mechanisms. The symbiosis between nudibranchs and Symbiodiniaceae has been identified as an efficacious model for examining these mechanisms, yet a comprehensive understanding of their histological structures and cellular processes remains elusive. A meticulous histological exploration of the nudibranch Pteraeolidia semperi, employing optical, fluorescence, and electron microscopy, has revealed fine tubules extending to the body surface, with associated epithelial cells having been shown to adeptly encapsulate Symbiodiniaceae intracellularly. By tracing the stages of the "bleaching" in nudibranchs, it was inferred that algal cells, translocated via the digestive gland, are directly phagocytosed and expelled by these epithelial cells. Collectively, these insights contribute substantially to the scholarly discourse on critical marine symbiotic associations.

Negative phototaxis in the photosymbiotic sea anemone Aiptasia as a potential strategy to protect symbionts from photodamage

Photosymbiotic cnidarians generally seek bright environments so that their symbionts can be photosynthetically active. However, excess light may result in a breakdown of symbiosis due to the accumulation of photodamage in symbionts causing symbiont loss (bleaching). It is currently unknown if photosymbiotic cnidarians sense light only to regulate spawning time and to facilitate predation, or whether they also use their light-sensing capacities to protect their symbionts from photodamage. In this study, we examined how the sea anemone Aiptasia changes its behaviour when exposed to excess light. We reveal that Aiptasia polyps, when carrying symbionts, contract their bodies when exposed to high light intensities and subsequently migrate away in a direction perpendicular to the light source. Interestingly, this negative phototaxis was only evident under blue light and absent upon UV, green and red light exposure. Non-symbiotic Aiptasia did not exhibit this light response. Our study demonstrates that photosymbiotic Aiptasia polyps display negative phototactic behaviour in response to blue light, and that they also can perceive its direction, despite lacking specialized eye structures. We postulate that Aiptasia uses blue light, which penetrates seawater efficiently, as a general proxy for sunlight exposure to protect its symbionts from photodamage.

Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil

Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes-urbanization and forest edge creation-on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new "suites" of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction-including increased greenhouse gas production-in temperate forest regions that are subsumed by urban expansion, both now and in the future.

Biodegradable Zein-Based Biocomposite Films for Underwater Delivery of Curcumin Reduce Thermal Stress Effects in Corals.

Massive coral bleaching episodes induced by thermal stress are one of the first causes of coral death worldwide. Overproduction of reactive oxygen species (ROS) has been identified as one of the potential causes of symbiosis breakdown between polyps and algae in corals during extreme heat wave events. Here, we propose a new strategy for mitigating heat effects by delivering underwater an antioxidant to the corals. We fabricated zein/polyvinylpyrrolidone (PVP)-based biocomposite films laden with the strong and natural antioxidant curcumin as an advanced coral bleaching remediation tool. Biocomposites' mechanical, water contact angle (WCA), swelling, and release properties can be tuned thanks to different supramolecular rearrangements that occur by varying the zein/PVP weight ratio. Following immersion in seawater, the biocomposites became soft hydrogels that did not affect the coral's health in the short (24 h) and long periods (15 days). Laboratory bleaching experiments at 29 and 33 °C showed that coral colonies of Stylophora pistillata coated with the biocomposites had ameliorated conditions in terms of morphological aspects, chlorophyll content, and enzymatic activity compared to untreated colonies and did not bleach. Finally, biochemical oxygen demand (BOD) confirmed the full biodegradability of the biocomposites, showing a low potential environmental impact in the case of open-field application. These insights may pave the way for new frontiers in mitigating extreme coral bleaching events by combining natural antioxidants and biocomposites.

High-frequency imagery to capture coral tissue (Montipora capricornis) response to environmental stress, a pilot study.

Environment stress is a major threat to the existence of coral reefs and has generated a lot of interest in the coral research community. Under the environmental stress, corals can experience tissue loss and/or the breakdown of symbiosis between the cnidarian host and its symbiotic algae causing the coral tissue to appear white as the skeleton can be seen by transparency. Image analysis is a common method used to assess tissue response under the environmental stress. However, the traditional approach is limited by the dynamic nature of the coral-algae symbiosis. Here, we observed coral tissue response in the scleractinian coral, Montipora capricornis, using high frequency image analysis throughout the experiment, as opposed to the typical start/end point assessment method. Color analysis reveals that the process can be divided into five stages with two critical stages according to coral tissue morphology and color ratio. We further explore changes to the morphology of individual polyps by means of the Pearson correlation coefficient and recurrence plots, where the quasi-periodic and nonstationary dynamics can be identified. The recurrence quantification analysis also allows the comparison between the different polyps. Our research provides a detailed visual and mathematical analysis of coral tissue response to environmental stress, which potentially shows universal applicability. Moreover, our approach provides a robust quantitative advancement for improving our insight into a suite of biotic responses in the perspective of coral health evaluation and fate prediction.

Engineered nanoceria alleviates thermally induced oxidative stress in free-living Breviolum minutum (Symbiodiniaceae, formerly Clade B)

The breakdown of symbiotic mutualism between cnidarian hosts and dinoflagellate algae partners (i.e., bleaching) has been linked to an immune-like response pathway brought on by a nitro-oxidative burst, a symptom of thermal stress. Stress induced by reactive oxygen species (ROS)/reactive nitrogen species is a problem common to aerobic systems. In this study, we tested the antioxidant effects of engineered poly(acrylic acid)-coated cerium dioxide nanoparticles (CeO2, nanoceria) on free-living Symbiodiniaceae (Breviolum minutum), a dinoflagellate alga that forms symbiotic relationships with reef-building corals and anemones. Results show that poly(acrylic acid)-coated CeO2 with hydrodynamic diameters of ~4 nm are internalized by B. minutum in under 30 min and subsequently localized in the cytosol. Nanoceria exposure does not inhibit cell growth over time, with the treated cultures showing a similar growth trend over the 25-day exposure. Aerobic activity and thermal stress when held at 34°C for 1 h (+6°C above control) led to increased intracellular ROS concentration with time. A clear ROS scavenging effect of the nanoceria was observed, with a 5-fold decrease in intracellular ROS levels during thermal stress. The nitric oxide (NO) concentration decreased by ~17% with thermal stress, suggesting the rapid involvement of NO scavenging enzymes or proteins within 1 h of stress onset. The presence of nanoceria did not appear to influence NO concentration. Furthermore, aposymbiotic anemones (Exaiptasia diaphana, ex Aiptasia pallida) were successfully infected with nanoceria-loaded B. minutum, demonstrating that inoculation could serve as a delivery method. The ability of nanoceria to be taken up by Symbiodiniaceae and reduce ROS production could be leveraged as a potential mitigation strategy to reduce coral bleaching.

Introduced galliforms as seed predators and dispersers in Hawaiian forests

In altered communities, novel species’ interactions may critically impact ecosystem functioning. One key ecosystem process, seed dispersal, often requires mutualistic interactions between frugivores and fruiting plants, and functional traits, such as seed width, may affect interaction outcomes. Forests of the Hawaiian Islands have experienced high species turnover, and introduced galliforms, the largest of the extant avian frugivores, consume fruit from both native and non-native plants. We investigated the roles of two galliform species as seed dispersers and seed predators in Hawaiian forests. Using captive Kalij Pheasants (Lophura leucomelanos) and Erckel’s Francolins (Pternistis erckelii), we measured the probability of seed survival during gut passage and seed germination following gut passage. We also examined which seeds are being dispersed in forests on the islands of O’ahu and Hawai’i. We found that galliforms are major seed predators for both native and non-native plants, with less than 5% of seeds surviving gut passage for all plants tested and in both bird species. Gut passage by Kalij Pheasants significantly reduced the probability of seeds germinating, especially for the native plants. Further, larger-seeded plants were both less likely to survive gut passage and to germinate. In the wild, galliforms dispersed native and non-native seeds at similar rates. Overall, our results suggest the introduced galliforms are a double-edged sword in conservation efforts; they may help reduce the spread of non-native plants, but they also destroy the seeds of some native plants. Broadly, we show mutualism breakdown may occur following high species turnover, and that functional traits can be useful for predicting outcomes from novel species’ interactions.

Coral and it's symbionts responses to the typical global marine pollutant BaP by 4D-Proteomics approach

The symbiosis of corals, zooxanthellae, and microbes is the foundation of the coral reef ecosystem. In addition to global warming, marine pollutants are another important factor causing the breakdown of coral symbiosis. Benzo(a)pyrene (BaP) is a globally widespread marine environmental pollutant that poses a severe threat to marine ecosystems. However, responses of coral symbionts to global marine pollutant stress remain unclear. In this study, we selected Acropora formosa as the target coral to explore its response to 50 μg L−1 BaP stress using diaPASEF proteomics and 16s rRNA microbiome analysis. The results showed that: 1) the coral symbionts were sensitive to BaP stress; 2) the photosynthetic system of zooxanthellae was crucial for the balance of symbiotic relationships; 3) the destruction of the photosynthetic system induced a zooxanthellae hypoxic stress response; 4) corals adapted to BaP stress by promoting non-essential protein degradation and changing energy metabolism strategies; 5) symbiotic bacteria showed strong adaptability to BaP. This study not only fills the gap in understanding the response mechanism of coral symbionts under BaP stress, but also provides fundamental data for coral reef protection strategies.

Thermal plasticity of coral reef symbionts is linked to major alterations in their lipidome composition

AbstractCoral bleaching caused by ocean warming is leading to worldwide coral decline. The physiological processes underlying this ecological event are still incompletely understood, although previous research has suggested oxidative stress as major player in the impairment of symbiont thylakoid membranes and in symbiosis breakdown. Lipids are interesting targets of investigation, given their susceptibility to thermal and oxidative stresses. Here, an untargeted lipidomic approach was employed to examine changes in lipidome and pigments of three coral reef symbionts (Symbiodiniaceae) after a heat shock in in vitro experiments. The acute thermal stress induced species‐specific changes in lipidome and pigments compositions of both heat sensitive and tolerant symbionts. Heat sensitivity was characterized by a steep and steady decline in cell densities over time (4 and 240 h after heat shock). At the membrane level, heat sensitive symbiont displayed a quantitative decrease in glycolipids linked to polyunsaturated fatty acids, followed by enrichment in oxidized lipids and sphingolipids. Despite showing distinct adaptations, the two heat tolerant symbionts were characterized by the preservation of membrane lipids after heat shock, particularly glycolipids. This finding suggests the action of powerful antioxidant systems, preventing the escalation of oxidized lipids concentration in thylakoid membranes under thermal stress. Although limited by the examination of free‐living symbionts, our study provides a solid baseline for the investigation of lipidome and pigments alterations of Symbiodiniaceae in response to heat stress. Novel potential lipid biomarkers linked to thermal stress are suggested. In particular, oxidized lipids—which are implicated in coral symbiosis establishment and breakdown—appear as attractive targets for further research.

Demographic consequences of mutualism disruption: Browsing and big-headed ant invasion drive acacia population declines.

Across the globe, biological invasions have disrupted mutualisms, producing reverberating consequences for ecosystems. Although invasive species frequently trigger mutualism disruptions, few studies have quantified the demographic mechanisms by which mutualism breakdown may generate population effects. In a Kenyan savanna, the invasive big-headed ant (Pheidole megacephala) has disrupted a foundational mutualism between the monodominant whistling-thorn tree (Acacia drepanolobium) and native ants (Crematogaster spp.) that deter browsing by large mammalian herbivores. We conducted experiments to quantify the demographic consequences of this mutualism disruption in the presence and absence of large mammalian herbivores. Invasion by P. megacephala exacerbated population declines of A. drepanolobium, primarily through decreased survival and reproduction of adult trees. However, these fitness reductions were small compared to those resulting from the presence of large mammalian herbivores, which negatively impacted growth and survival. Contrary to expectation, the expulsion of metabolically costly Crematogaster mutualists by P. megacephala did not result in higher population growth rates for trees protected from large mammalian herbivores. Our results suggest that invasive P. megacephala may impose a direct metabolic cost to trees exceeding that of native mutualists while providing no protection from browsing by large mammalian herbivores. Across landscapes, we expect that invasion by P. megacephala will reduce A. drepanolobium populations, but that the magnitude and demographic pathways of this effect will hinge on the presence and abundance of browsers.

Bleaching physiology: who's the 'weakest link' - host vs. symbiont?

Environmental stress, such as an increase in the sea surface temperature, triggers coral bleaching, a profound dysfunction of the mutualist symbiosis between the host cnidarians and their photosynthetic dinoflagellates of the Family Symbiodiniaceae. Because of climate change, mass coral bleaching events will increase in frequency and severity in the future, threatening the persistence of this iconic marine ecosystem at global scale. Strategies adapted to coral reefs preservation and restoration may stem from the identification of the succession of events and of the different molecular and cellular contributors to the bleaching phenomenon. To date, studies aiming to decipher the cellular cascade leading to temperature-related bleaching, emphasized the involvement of reactive species originating from compromised bioenergetic pathways (e.g. cellular respiration and photosynthesis). These molecules are responsible for damage to various cellular components causing the dysregulation of cellular homeostasis and the breakdown of symbiosis. In this review, we synthesize the current knowledge available in the literature on the cellular mechanisms caused by thermal stress, which can initiate or participate in the cell cascade leading to the loss of symbionts, with a particular emphasis on the role of each partner in the initiating processes.

Patchy Distribution of GTPases of Immunity-Associated Proteins (GIMAP) within Cnidarians and Dinoflagellates Suggests a Complex Evolutionary History.

GTPases of Immunity-Associated Proteins (GIMAP) are a group of small GTP-binding proteins found in a variety of organisms, including vertebrates, invertebrates, and plants. These proteins are characterized by the highly conserved AIG1 domain, and in vertebrates, have been implicated in regulation of the immune system as well as apoptosis and autophagy, though their exact mechanism of action remains unclear. Recent work on cnidarian GIMAPs suggests a conserved role in immunity, apoptosis, and autophagy—three processes involved in coral bleaching, or the breakdown of cnidarian-dinoflagellate symbiosis. Therefore, to further understand the evolution of GIMAPs in this group of organisms, the purpose of this study was to characterize GIMAP or GIMAP-like sequences utilizing publicly available genomic and transcriptomic data in species across the cnidarian phylogeny. The results revealed a patchy distribution of GIMAPs in cnidarians, with three distinct types referred to as L-GIMAP, S-GIMAP, and GIMAP-like. Additionally, GIMAPs were present in most dinoflagellate species and formed seven well-supported clades. Overall, these results elucidate the distribution of GIMAPs within two distantly related eukaryotic groups and represent the first in-depth investigation on the evolution of these proteins within both protists and basal metazoans.

Increased temperature reduces the positive effect of sulfide-detoxification mutualism on Zostera noltii nutrient uptake and growth

Seagrass meadows form essential ecological components in coastal zones but are rapidly declining worldwide due to anthropogenic impacts, including eutrophication and climate change-related heat waves. An important consequence of increased eutrophication is organic matter input in the sediment, which, together with raised temperatures, stimulates the production of toxic sulfide. Although multiple recent studies have highlighted that seagrass can engage in a mutualistic relationship with lucinid bivalves alleviating sulfide toxicity in the rhizosphere, it remains unclear how this mutualism is affected by temperature and eutrophication. To unravel this relation, we investigated the response of the seagrass Zostera noltii to contrasting sediment organic matter conditions, temperatures and presence/absence of the lucinid clam Loripes orbiculatus in a full-factorial mesocosm experiment. Results demonstrate that temperature increased porewater sulfide and nutrient levels, particularly in treatments with high sediment organic matter content. Interestingly, L. orbiculatus reduced not only sulfide levels, but also porewater nutrients. The removal of sulfide in turn stimulated Z. noltii growth, despite lower nutrient availability. Finally, increased temperature suppressed the mutualistic benefit for Z. noltii as sulfide detoxification became hampered. We conclude that, as eutrophication remains an issue in the coastal zone and temperature extremes will likely become more common in the future, seagrass meadows where lucinids occur may need to increasingly rely on this mutualism. At the same time, however, this interaction will become more strained, with an inherent increasing risk of mutualism breakdown.

Viral-Like Particles Are Associated With Endosymbiont Pathology in Florida Corals Affected by Stony Coral Tissue Loss Disease

Stony coral tissue loss disease (SCTLD) was first documented in 2014 near the Port of Miami, Florida, and has since spread north and south along Florida’s Coral Reef, killing large numbers of more than 20 species of coral and leading to the functional extinction of at least one species, Dendrogyra cylindrus. SCTLD is assumed to be caused by bacteria based on presence of different molecular assemblages of bacteria in lesioned compared to apparently healthy tissues, its apparent spread among colonies, and cessation of spread of lesions in individual colonies treated with antibiotics. However, light microscopic examination of tissues of corals affected with SCTLD has not shown bacteria associated with tissue death. Rather, microscopy shows dead and dying coral cells and symbiotic dinoflagellates (endosymbionts) indicating a breakdown of host cell and endosymbiont symbiosis. It is unclear whether host cells die first leading to death of endosymbionts or vice versa. Based on microscopy, hypotheses as to possible causes of SCTLD include infectious agents not visible at the light microscopy level or toxicosis, perhaps originating from endosymbionts. To clarify this, we examined corals affected with SCTLD and apparently healthy corals using transmission electron microscopy. Endosymbionts in SCTLD-affected and apparently healthy corals consistently had varying degrees of pathology associated with elongated particles compatible in morphology with filamentous positive single-stranded RNA viruses of plants termed anisometric viral-like particles (AVLP). There was apparent progression from early to late replication of AVLP in the cytoplasm of endosymbionts adjacent to or at times within chloroplasts, with morphologic changes in chloroplasts consistent with those seen in plant cells infected by viruses. Coral host cell pathology appeared limited to massive proliferation and lysis of mucus cells. Based on these findings, we hypothesize that SCTLD is a viral disease of endosymbionts leading to coral host death. Efforts to confirm the presence of a virus associated with SCTLD through other means would be appropriate. These include showing the presence of a virus through molecular assays such as deep sequencing, attempts to grow this virus in the laboratory through culture of endosymbionts, localization of virus in tissue sections using immunohistochemistry or in situ hybridization, and experimental infection of known-virus-negative corals to replicate disease at the gross and microscopic level.

Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora

Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.

Shifts between cooperation and antagonism driven by individual variation: a systematic synthesis review

The outcomes of interspecific and intraspecific ecological interactions can be considered to fall along continua from cooperative (mutually beneficial) to antagonistic (detrimental to one or both parties). Furthermore, the position of an interaction outcome along the continuum, for example whether a symbiont provides net costs or benefits to its host, or whether two conspecifics cooperatively forage or compete for food, is often not fixed but can change over time or across contexts. In this systematic review, we investigate the role of intraspecific trait variation (‘ITV') in one or both interacting parties in determining the cooperative‐antagonistic outcome of inter‐ and intraspecific ecological interactions. Based on a literature collection of 96 empirical and theoretical publications meeting our inclusion criteria, we give an overview of the types of interaction continua involved; traits related to outcome variance; and mechanisms as well as constraints on shifts in interactions outcomes. We propose that ITV can lead to shifts in interaction outcomes via two interrelated mechanisms. First,trait frequency effectsoccur when there are changes in a population's composition of traits linked to cooperation or antagonism (e.g. aggressive personality types, cheater phenotypes etc.), leading to net shifts in interaction outcomes. Second,systemic variance effectsoccur where the level of ITV in a trait in a population (as opposed to the mean value) is the factor that influences the cooperative‐antagonistic outcome. Heritable trait differences and phenotypic plasticity are sources of phenotypic variation among individuals, and both the degree of heritability and plasticity of the trait involved may determine whether shifts between cooperation and antagonism are likely to be short‐term (i.e. context‐dependent) or lead to more persistent shifts (e.g. mutualism breakdown). To guide future research, we describe knowledge gaps and divergences between empirical and theoretical literature, highlighting the value of applying evidence synthesis methods in ecology and evolution.

Rapid compensatory evolution can rescue low fitness symbioses following partner switching

Partner switching plays an important role in the evolution of symbiosis, enabling local adaptation and recovery from the breakdown of symbiosis. Because of intergenomic epistasis, partner-switched symbioses may possess novel combinations of phenotypes but may also exhibit low fitness due to their lack of recent coevolutionary history. Here, we examine the structure and mechanisms of intergenomic epistasis in the Paramecium-Chlorella symbiosis and test whether compensatory evolution can rescue initially low fitness partner-switched symbioses. Using partner-switch experiments coupled with metabolomics, we show evidence for intergenomic epistasis wherein low fitness is associated with elevated symbiont stress responses either in dark or high irradiance environments, potentially owing to mismatched light management traits between the host and symbiont genotypes. Experimental evolution under high light conditions revealed that an initially low fitness partner-switched non-native host-symbiont pairing rapidly adapted, gaining fitness equivalent to the native host-symbiont pairing in less than 50 host generations. Compensatory evolution took two alternative routes: either hosts evolved higher symbiont loads to mitigate for their new algal symbiont's poor performance, or the algal symbionts themselves evolved higher investment in photosynthesis and photoprotective traits to better mitigate light stress. These findings suggest that partner switching combined with rapid compensatory evolution can enable the recovery and local adaptation of symbioses in response to changing environments.