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Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, Astrangia poculata.

ABSTRACT: Scleractinian corals are essential ecosystem engineers, forming the basis of coral reef ecosystems. However, these organisms are in decline globally, in part due to rising disease prevalence. Most corals are dependent on symbiotic interactions with single-celled algae from the family Symbiodiniaceae to meet their nutritional needs, however, suppression of host immunity may be essential to this relationship. To explore immunological consequences of algal symbioses in scleractinian corals, we investigated constitutive immune activity in the facultatively symbiotic coral, Astrangia poculata. We compared immune metrics (melanin synthesis, antioxidant production and antibacterial activity) between coral colonies of varying symbiont density. Symbiont density was positively correlated to both antioxidant activity and melanin concentration, likely as a result of the dual roles of these pathways in immunity and symbiosis regulation. Our results confirm the complex nature of relationships between algal symbiosis and host immunity and highlight the need for nuanced approaches when considering these relationships.

SUBMITTER: Changsut I

PROVIDER: S-EPMC9667134 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, <i>Astrangia poculata</i>.

Changsut Isabella I Womack Haley R HR Shickle Alicia A Sharp Koty H KH Fuess Lauren E LE

Biology letters 20221116 11

Scleractinian corals are essential ecosystem engineers, forming the basis of coral reef ecosystems. However, these organisms are in decline globally, in part due to rising disease prevalence. Most corals are dependent on symbiotic interactions with single-celled algae from the family Symbiodiniaceae to meet their nutritional needs, however, suppression of host immunity may be essential to this relationship. To explore immunological consequences of algal symbioses in scleractinian corals, we inve ...[more]

PMID: 36382375

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Project description:BackgroundUnderstanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiome associations are beneficial, yet the mechanisms that determine the composition of the coral microbiome remain largely unknown. Here, we characterized microbiome diversity in the temperate, facultatively symbiotic coral Astrangia poculata at four seasonal time points near the northernmost limit of the species range. The facultative nature of this system allowed us to test seasonal influence and symbiotic state (Symbiodinium density in the coral) on microbiome community composition.ResultsChange in season had a strong effect on A. poculata microbiome composition. The seasonal shift was greatest upon the winter to spring transition, during which time A. poculata microbiome composition became more similar among host individuals. Within each of the four seasons, microbiome composition differed significantly from that of surrounding seawater but was surprisingly uniform between symbiotic and aposymbiotic corals, even in summer, when differences in Symbiodinium density between brown and white colonies are the highest, indicating that the observed seasonal shifts are not likely due to fluctuations in Symbiodinium density.ConclusionsOur results suggest that symbiotic state may not be a primary driver of coral microbial community organization in A. poculata, which is a surprise given the long-held assumption that excess photosynthate is of importance to coral-associated microbes. Rather, other environmental or host factors, in this case, seasonal changes in host physiology associated with winter quiescence, may drive microbiome diversity. Additional studies of A. poculata and other facultatively symbiotic corals will provide important comparisons to studies of reef-building tropical corals and therefore help to identify basic principles of coral microbiome assembly, as well as functional relationships among holobiont members.

Project description:The microbiome of the temperate coral Astrangia poculata was first described in 2017 using next-generation Illumina sequencing to examine the coral's bacterial and archaeal associates across seasons and among hosts of differing symbiotic status. To assess the impact of methodology on the detectable diversity of the coral's microbiome, we obtained near full-length Sanger sequences from clone libraries constructed from a subset of the same A. poculata samples. Eight samples were analyzed: two sets of paired symbiotic (brown) and aposymbiotic (white) colonies collected in the fall (September) and two sets collected in the spring (April). Analysis of the Sanger sequences revealed that the microbiome of A. poculata exhibited a high level of richness; 806 OTUs were identified among 1390 bacterial sequences. While the Illumina study revealed that A. poculata's microbial communities did not significantly vary according to symbiotic state, but did vary by season, Sanger sequencing did not expose seasonal or symbiotic differences in the microbiomes. Proteobacteria dominated the microbiome, forming the majority (55% to 80%) of classifiable bacteria in every sample, and the five bacterial classes with the highest mean relative portion (5% to 35%) were the same as those determined by prior Illumina sequencing. Sanger sequencing also captured the same core taxa previously identified by next-generation sequencing. Alignment of all sequences and construction of a phylogenetic tree revealed that both sequencing methods provided similar portrayals of the phylogenetic diversity within A. poculata's bacterial associates. Consistent with previous findings, the results demonstrated that the Astrangia microbiome is stable notwithstanding the choice of sequencing method and the far fewer sequences generated by clone libraries (46 to 326 sequences per sample) compared to next-generation sequencing (3634 to 48481 sequences per sample). Moreover, the near-full length 16S rRNA sequences produced by this study are presented as a resource for the community studying this model system since they provide necessary information for designing primers and probes to further our understanding of this coral's microbiome.

Project description:The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a 2-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, or translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis.

Dataset Information

Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, Astrangia poculata.

Publications

Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, <i>Astrangia poculata</i>.

Similar Datasets

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