Cladocopium community divergence in two Acropora coral hosts across multiple spatial scales

AbstractMany broadly-dispersing corals acquire their algal symbionts (Symbiodiniaceae) ‘horizontally’ from their environment upon recruitment. Horizontal transmission could promote coral fitness across diverse environments provided that corals can associate with divergent algae across their range and that these symbionts exhibit reduced dispersal potential. Here we quantified community divergence of Cladocopium algal symbionts in two coral host species (Acropora hyacinthus, Acropora digitifera) across two spatial scales (reefs on the same island, and between islands) across the Micronesian archipelago using microsatellites. We find that both hosts associated with two genetically distinct Cladocopium lineages (C40, C21), confirming that Acropora coral hosts associate with a range of Cladocopium symbionts across this region. Both C40 and C21 exhibited extensive clonality. Clones not only existed across host conspecifics living on the same reef, but also spanned host species, reef sites within islands, and even different islands. Both Cladocopium lineages exhibited moderate host specialization and divergence across islands. In addition, within every island, algal symbiont communities were significantly clustered by both host species and reef site, highlighting that coral-associated Cladocopium communities are structured across small spatial scales and within hosts on the same reef. This is in stark contrast to their coral hosts, which never exhibited significant genetic divergence between reefs on the same island. These results support the view that horizontal transmission could improve local fitness for broadly dispersing Acropora coral species.

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Ecological factors rather than barriers to dispersal shape genetic structure of algal symbionts in horizontally-transmitting corals

10.1101/037994 ◽

2016 ◽

Cited By ~ 4

Author(s):

SW Davies ◽

FC Wham ◽

MR Kanke ◽

MV Matz

Keyword(s):

Genetic Structure ◽

Host Species ◽

Coral Species ◽

Spatial Scales ◽

Horizontal Transmission ◽

Ecological Factors ◽

Local Environment ◽

Transmission Strategy ◽

Algal Symbionts ◽

Genetic Structures

AbstractMany reef-building corals acquire their algal symbionts (Symbiodinium sp.) from the local environment upon recruitment. This horizontal transmission strategy where hosts pair with locally available symbionts could serve to increase coral fitness across diverse environments, as long as hosts maintain high promiscuity and symbionts adapt locally. Here, we tested this hypothesis in two coral species by comparing host and symbiont genetic structures across different spatial scales in Micronesia. Each host species associated with two genetically distinct Symbiodinium lineages, confirming high promiscuity in broadly dispersing hosts. However, contrary to our initial expectation, symbiont genetic structure was independent of physical barriers to dispersal between islands, unlike genetic structure of their hosts that was nearly perfectly explained by ocean currents. Instead, Symbiodinium consistently demonstrated genetic divergence among local reefs and between the two host species at each island, although not necessarily between distant islands. These observations indicate that Symbiodinium lineages disperse much more broadly than previously thought and continuously adapt to specific hosts and reef environments across their range, following the classical Baas Becking’s hypothesis: “Everything is everywhere, but the environment selects”. Overall, our findings confirm that horizontal transmission could be a mechanism for broadly dispersing coral species to enhance their local fitness by associating with locally adapted symbionts. Dramatic differences in factors driving the genetic structures of horizontally-transmitting corals and their Symbiodinium imply that viewing their combined genomes as a single entity (‘hologenome’) would not be useful in the context of their evolution and adaptation.

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An algal symbiont (Breviolum psygmophilum) responds more strongly to chronic high temperatures than its facultatively symbiotic coral host (Astrangia poculata)

10.1101/2021.02.08.430325 ◽

2021 ◽

Author(s):

Andrea N. Chan ◽

Luis A. González-Guerrero ◽

Roberto Iglesias-Prieto ◽

Elizabeth M. Burmester ◽

Randi D. Rotjan ◽

...

Keyword(s):

Heat Stress ◽

Thermal Stress ◽

Stress Response ◽

Coral Bleaching ◽

Scleractinian Corals ◽

Coral Host ◽

Algal Symbionts ◽

Algal Symbiont ◽

Astrangia Poculata ◽

And Control

AbstractScleractinian corals form the foundation of coral reefs by secreting skeletons of calcium carbonate. Their intracellular algal symbionts (Symbiodiniaceae) translocate a large proportion of photosynthate to the coral host, which is required to maintain high rates of calcification. Global warming is causing dissociation of coral host and algal symbiont, visibly presented as coral bleaching. Despite decades of study, the precise mechanisms of coral bleaching remain unknown. Separating the thermal stress response of the coral from the algal symbiont is key to understanding bleaching in tropical corals. The facultatively symbiotic northern star coral, Astrangia poculata, naturally occurs as both symbiotic and aposymbiotic (lacking algal symbionts) polyps – sometimes on the same coral colony. Thus, it is possible to separate the heat stress response of the coral host alone from the coral in symbiosis with its symbiont Breviolum psygmophilum. Using replicate symbiotic and aposymbiotic ramets of A. poculata, we conducted a chronic heat stress experiment to increase our understanding of the cellular mechanisms resulting in coral bleaching. Sustained high temperature stress resulted in photosynthetic dysfunction in B. psygmophilum, including a decline in maximum photosynthesis rate, maximum photochemical efficiency, and the absorbance peak of chlorophyll a. Interestingly, the metabolic rates of symbiotic and aposymbiotic corals were differentially impacted. RNAseq analysis revealed more differentially expressed genes between heat-stressed and control aposymbiotic colonies than heat-stressed and control symbiotic colonies. Notably, aposymbiotic colonies increased the expression of inflammation-associated genes such as nitric oxide synthases. Unexpectedly, the largest transcriptional response was observed between heat-stressed and control B. psygmophilum, including genes involved in photosynthesis, response to oxidative stress, and meiosis. Thus, it appears that the algal symbiont suppresses the immune response of the host, potentially increasing the vulnerability of the host to pathogens. The A. poculata-B. psygmophilum symbiosis provides a tractable model system for investigating thermal stress and immune challenge in scleractinian corals.

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Recruit symbiosis establishment and Symbiodiniceae composition influenced by adult corals and reef sediment

10.1101/421339 ◽

2018 ◽

Author(s):

A Ali ◽

N Kriefall ◽

LE Emery ◽

CD Kenkel ◽

MV Matz ◽

...

Keyword(s):

Life Cycle ◽

Horizontal Transmission ◽

Alpha Diversity ◽

Chemical Signaling ◽

Transmission Strategy ◽

Juvenile Coral ◽

Algal Symbionts ◽

Surrounding Environment ◽

Algal Symbiont

ABSTRACTFor most reef-building corals, the establishment of symbiosis occurs via horizontal transmission, where juvenile coral recruits acquire their algal symbionts (family Symbiodiniaceae) from their surrounding environment post-settlement. This transmission strategy allows corals to interact with a diverse array of symbionts, potentially facilitating adaptation to the newly settled environment. We exposed aposymbiotic Pseudodiploria strigosa recruits from the Flower Garden Banks to natal reef sediment (C-S+), symbiotic adult coral fragments (C+S-), sediment and coral fragments (C+S+), or seawater controls (C-S-) and quantified rates of symbiont uptake and Symbiodiniaceae community composition within each recruit using metabarcoding of the ITS2 locus. The most rapid uptake was observed in C+S+ treatments and this combination also led to the highest symbiont alpha diversity in recruits. While C-S+ treatments exhibited the next highest uptake rate, only one individual recruit successfully established symbiosis in the C+S-treatment, suggesting that sediment both serves as a direct symbiont source for coral recruits and promotes (or, potentially, mediates) transmission from adult coral colonies. In turn, presence of adult corals facilitated uptake from the sediment, perhaps via chemical signaling. Taken together, our results reinforce the key role of sediment in algal symbiont uptake by P. strigosa recruits and suggest that sediment plays a necessary, but perhaps not sufficient, role in the life cycle of the algal Symbiodinaceae symbionts.

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Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events

10.1101/2020.07.24.219766 ◽

2020 ◽

Author(s):

Jenna Dilworth ◽

Carlo Caruso ◽

Valerie A. Kahkejian ◽

Andrew C. Baker ◽

Crawford Drury

Keyword(s):

Thermal Stress ◽

Community Composition ◽

Photochemical Efficiency ◽

Coral Host ◽

Host Genotype ◽

Reef Environment ◽

Montipora Capitata ◽

Algal Symbionts ◽

Algal Symbiont ◽

Photochemical Damage

AbstractAs sea surface temperatures increase worldwide due to climate change, coral bleaching events are becoming more frequent and severe, resulting in reef degradation. Leveraging the inherent ability of reef-building corals to acclimatize to thermal stress via pre-exposure to protective temperature treatments may become an important tool in improving the resilience of coral reefs to rapid environmental change. We investigated whether historical bleaching phenotype, coral host genotype, and exposure to protective temperature treatments would affect the response of the Hawaiian coral Montipora capitata to natural thermal stress. Fragments were collected from colonies that demonstrated different bleaching responses during the 2014-2015 event in Kāne’ohe Bay (O’ahu, Hawai’i) and exposed to four different artificial temperature pre-treatments (and a control at ambient temperature). After recovery, fragments experienced a natural thermal stress event either in laboratory conditions or their native reef environment. Response to thermal stress was quantified by measuring changes in the algal symbionts’ photochemical efficiency, community composition, and relative density. Historical bleaching phenotype was reflected in stable differences in symbiont community composition, with historically bleached corals containing only Cladocopium symbionts and historically non-bleached corals having mixed symbiont communities dominated by Durusdinium. Mixed-community corals lost more Cladocopium than Cladocopium-only corals during the natural thermal stress event, and preferentially recovered with Durusdinium. Laboratory pre-treatments exposed corals to more thermal stress than anticipated, causing photochemical damage that varied significantly by genotype. While none of the treatments had a protective effect, temperature variation during treatments had a significant detrimental effect on photochemical efficiency during the thermal stress event. These results show that acclimatization potential is affected by fine-scale differences in temperature regime, host genotype, and relatively stable differences in symbiont community composition that underpin historical bleaching phenotypes in M. capitata.

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The coral symbiont Candidatus Aquarickettsia is variably abundant in threatened Caribbean acroporids and transmitted horizontally

The ISME Journal ◽

10.1038/s41396-021-01077-8 ◽

2021 ◽

Author(s):

Lydia J. Baker ◽

Hannah G. Reich ◽

Sheila A. Kitchen ◽

J. Grace Klinges ◽

Hanna R. Koch ◽

...

Keyword(s):

Positive Selection ◽

Coral Disease ◽

Horizontal Transmission ◽

Geographic Location ◽

Geographic Region ◽

Pcr Analysis ◽

Coral Host ◽

Acropora Cervicornis ◽

Coral Colony ◽

Algal Symbiont

AbstractThe symbiont “Candidatus Aquarickettsia rohweri” infects a diversity of aquatic hosts. In the threatened Caribbean coral, Acropora cervicornis, Aquarickettsia proliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality of coral. This study evaluated the extent, as well as the ecology and evolution of Aquarickettsia infecting threatened corals, Ac. cervicornis, and Ac. palmata and their hybrid (“Ac. prolifera”). Aquarickettsia was found in all acroporids, with coral host and geographic location impacting the infection magnitude. Phylogenomic and genome-wide single-nucleotide variant analysis of Aquarickettsia found phylogenetic clustering by geographic region, not by coral taxon. Analysis of Aquarickettsia fixation indices suggests multiple sequential infections of the same coral colony are unlikely. Furthermore, relative to other Rickettsiales species, Aquarickettsia is undergoing positive selection, with Florida populations experiencing greater positive selection relative to other Caribbean locations. This may be due in part to Aquarickettsia proliferating in response to greater nutrient stress in Florida, as indicated by greater in situ replication rates in these corals. Aquarickettsia was not found to significantly codiversify with either the coral animal or the coral’s algal symbiont (Symbiodinium “fitti”). Quantitative PCR analysis showed that gametes, larvae, recruits, and juveniles from susceptible, captive-reared coral genets were not infected with Aquarickettsia. Thus, horizontal transmission of Aquarickettsia via coral mucocytes or an unidentified host is more likely. The prevalence of Aquarickettsia in Ac. cervicornis and its high abundance in the Florida coral population suggests that coral disease mitigation efforts focus on preventing early infection via horizontal transmission.

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The dilution effect limits plasmid horizontal transmission in multispecies bacterial communities

Microbiology ◽

10.1099/mic.0.001086 ◽

2021 ◽

Vol 167 (9) ◽

Author(s):

Anastasia Kottara ◽

Laura Carrilero ◽

Ellie Harrison ◽

James P. J. Hall ◽

Michael A. Brockhurst

Keyword(s):

Host Species ◽

Bacterial Communities ◽

Horizontal Transmission ◽

Dilution Effect ◽

Infection Risk ◽

Host Cells ◽

Evolutionary Innovation ◽

Genomic Divergence ◽

Plasmid Diversity ◽

Plasmid Conjugation

By transferring ecologically important traits between species, plasmids drive genomic divergence and evolutionary innovation in their bacterial hosts. Bacterial communities are often diverse and contain multiple coexisting plasmids, but the dynamics of plasmids in multi-species communities are poorly understood. Here, we show, using experimental multi-species communities containing two plasmids, that bacterial diversity limits the horizontal transmission of plasmids due to the ‘dilution effect’; this is an epidemiological phenomenon whereby living alongside less proficient host species reduces the expected infection risk for a focal host species. In addition, plasmid horizontal transmission was also affected by plasmid diversity, such that the rate of plasmid conjugation was reduced from co-infected host cells carrying both plasmids. In diverse microbial communities, plasmid spread may be limited by the dilution effect and plasmid–plasmid interactions, reducing the rate of horizontal transmission.

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Unique combinations of coral host and algal symbiont genotypes reflect intraspecific variation in heat stress responses among colonies of the reef-building coral, Montipora digitata

Marine Biology ◽

10.1007/s00227-019-3632-z ◽

2020 ◽

Vol 167 (2) ◽

Cited By ~ 2

Author(s):

Javid Kavousi ◽

Vianney Denis ◽

Victoria Sharp ◽

James Davis Reimer ◽

Takashi Nakamura ◽

...

Keyword(s):

Heat Stress ◽

Intraspecific Variation ◽

Stress Responses ◽

Coral Host ◽

Algal Symbiont

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Flexibility of nutritional strategies within a mutualism: food availability affects algal symbiont productivity in two congeneric sea anemone species

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.1860 ◽

2020 ◽

Vol 287 (1940) ◽

pp. 20201860

Author(s):

Samuel A. Bedgood ◽

Sarah E. Mastroni ◽

Matthew E. S. Bracken

Keyword(s):

Food Availability ◽

Sea Anemone ◽

Symbiotic Association ◽

Sea Anemones ◽

External Resources ◽

Carbon And Nitrogen ◽

Algal Symbionts ◽

Algal Symbiont ◽

Nutritional Strategy ◽

Nutritional Strategies

Mutualistic symbioses are common, especially in nutrient-poor environments where an association between hosts and symbionts can allow the symbiotic partners to persist and collectively out-compete non-symbiotic species. Usually these mutualisms are built on an intimate transfer of energy and nutrients (e.g. carbon and nitrogen) between host and symbiont. However, resource availability is not consistent, and the benefit of the symbiotic association can depend on the availability of resources to mutualists. We manipulated the diets of two temperate sea anemone species in the genus Anthopleura in the field and recorded the responses of sea anemones and algal symbionts in the family Symbiodiniaceae to our treatments. Algal symbiont density, symbiont volume and photosynthetic efficiency of symbionts responded to changes in sea anemone diet, but the responses depended on the species of sea anemone. We suggest that temperate sea anemones and their symbionts can respond to changes in anemone diet, modifying the balance between heterotrophy and autotrophy in the symbiosis. Our data support the hypothesis that symbionts are upregulated or downregulated based on food availability, allowing for a flexible nutritional strategy based on external resources.

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Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus

Environmental Chemistry ◽

10.1071/en15023 ◽

2016 ◽

Vol 13 (2) ◽

pp. 252 ◽

Cited By ~ 17

Author(s):

P. R. Frade ◽

V. Schwaninger ◽

B. Glasl ◽

E. Sintes ◽

R. W. Hill ◽

...

Keyword(s):

Host Species ◽

Community Dynamics ◽

Sulfur Compound ◽

Quantitative Polymerase Chain Reaction ◽

Sulfur Compounds ◽

Microbial Processes ◽

Coral Host ◽

Gene Abundance ◽

Coral Surface ◽

Degrading Bacteria

Environmental context Corals produce copious amounts of dimethylsulfoniopropionate (DMSP), a sulfur compound implicated in climate regulation. We studied DMSP concentrations inside corals and unveiled the linkage between DMSP availability and the abundance of DMSP-degrading bacterial groups inhabiting the corals’ surface. Our findings suggest that DMSP mediates the interplay between corals and microbes, highlighting the importance of sulfur compounds for microbial processes in corals and for the resilience of coral reef ecosystems. Abstract Corals produce copious amounts of dimethylsulfoniopropionate (DMSP), a sulfur compound thought to play a role in structuring coral-associated bacterial communities. We tested the hypothesis that a linkage exists between DMSP availability in coral tissues and the community dynamics of bacteria in coral surface mucus. We determined DMSP concentrations in three coral species (Meandrina meandrites, Porites astreoides and Siderastrea siderea) at two sampling depths (5 and 25m) and times of day (dawn and noon) at Curaçao, Southern Caribbean. DMSP concentration (4–409nmolcm–2 coral surface) varied with host species-specific traits such as Symbiodinium cell abundance, but not with depth or time of sampling. Exposure of corals to air caused a doubling of their DMSP concentration. The phylogenetic affiliation of mucus-associated bacteria was examined by clone libraries targeting three main subclades of the bacterial DMSP demethylase gene (dmdA). dmdA gene abundance was determined by quantitative Polymerase Chain Reaction (qPCR) against a reference housekeeping gene (recA). Overall, a higher availability of DMSP corresponded to a lower relative abundance of the dmdA gene, but this pattern was not uniform across all host species or bacterial dmdA subclades, suggesting the existence of distinct DMSP microbial niches or varying dmdA DMSP affinities. This is the first study quantifying dmdA gene abundance in corals and linking related changes in the community dynamics of DMSP-degrading bacteria to DMSP availability. Our study suggests that DMSP mediates the regulation of microbes by the coral host and highlights the significance of sulfur compounds for microbial processes in coral reefs.

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