Lineage-specific variation in the evolutionary stability of coral photosymbiosis.
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ABSTRACT:
SUBMITTER: Gault JA
PROVIDER: S-EPMC8457658 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundScleractinian corals of the genus Montipora (Anthozoa, Cnidaria) possess some unusual biological traits, such as vertical transmission of algal symbionts; however, the genetic bases for those traits remain unknown. We performed extensive comparative genomic analyses among members of the family Acroporidae (Montipora, Acropora, and Astreopora) to explore genomic novelties that might explain unique biological traits of Montipora using improved genome assemblies and gene predictions for M. cactus, M. efflorescens and Astreopora myriophthalma.ResultsWe obtained genomic data for the three species of comparable high quality to other published coral genomes. Comparative genomic analyses revealed that the gene families restricted to Montipora are significantly more numerous than those of Acropora and Astreopora, but their functions are largely unknown. The number of gene families specifically expanded in Montipora was much lower than the number specifically expanded in Acropora. In addition, we found that evolutionary rates of the Montipora-specific gene families were significantly higher than other gene families shared with Acropora and/or Astreopora. Of 40 gene families under positive selection (Ka/Ks ratio > 1) in Montipora, 30 were specifically detected in Montipora-specific gene families. Comparative transcriptomic analysis of early life stages of Montipora, which possesses maternally inherited symbionts, and Acropora, which lacks them, revealed that most gene families continuously expressed in Montipora, but not expressed in Acropora do not have orthologs in Acropora. Among the 30 Montipora-specific gene families under positive selection, 27 are expressed in early life stages.ConclusionsLineage-specific gene families were important to establish the genus Montipora, particularly genes expressed throughout early life stages, which under positive selection, gave rise to biological traits unique to Montipora. Our findings highlight evolutionarily acquired genomic bases that may support symbiosis in these stony corals and provide novel insights into mechanisms of coral-algal symbiosis, the physiological foundation of coral reefs.
| S-EPMC9145168 | biostudies-literature
Project description:BackgroundOcean warming is a leading cause of increasing episodes of coral bleaching, the dissociation between coral hosts and their dinoflagellate algal symbionts in the family Symbiodiniaceae. While the diversity and flexibility of Symbiodiniaceae is presumably responsible for variations in coral response to physical stressors such as elevated temperature, there is little data directly comparing physiological performance that accounts for symbiont identity associated with the same coral host species. Here, using Pocillopora damicornis harboring genotypically distinct Symbiodiniaceae strains, we examined the physiological responses of the coral holobiont and the dynamics of symbiont community change under thermal stress in a laboratory-controlled experiment.ResultsWe found that P. damicornis dominated with symbionts of metahaplotype D1-D4-D6 in the genus Durusdinium (i.e., PdD holobiont) was more robust to thermal stress than its counterpart with symbionts of metahaplotype C42-C1-C1b-C1c in the genus Cladocopium (i.e., PdC holobiont). Under ambient temperature, however, the thermally sensitive Cladocopium spp. exhibited higher photosynthetic efficiency and translocated more fixed carbon to the host, likely facilitating faster coral growth and calcification. Moreover, we observed a thermally induced increase in Durusdinium proportion in the PdC holobiont; however, this "symbiont shuffling" in the background was overwhelmed by the overall Cladocopium dominance, which coincided with faster coral bleaching and reduced calcification.ConclusionsThese findings support that lineage-specific symbiont dominance is a driver of distinct coral responses to thermal stress. In addition, we found that "symbiont shuffling" may begin with stress-forced, subtle changes in the rare biosphere to eventually trade off growth for increased resilience. Furthermore, the flexibility in corals' association with thermally tolerant symbiont lineages to adapt or acclimatize to future warming oceans should be viewed with conservative optimism as the current rate of environmental changes may outpace the evolutionary capabilities of corals. Video Abstract.
| S-EPMC10521517 | biostudies-literature
Project description:Comparison of the human genome with other primates offers the opportunity to detect evolutionary events that created the diverse phenotypes among the primate species. Because the primate genomes are highly similar to one another, methods developed for analysis of more divergent species do not always detect signs of evolutionary selection.We have developed a new method, called DivE, specifically designed to find regions that have evolved either more or less rapidly than expected, for any clade within a set of very closely related species. Unlike some previous methods, DivE does not rely on rates of synonymous and nonsynonymous substitution, which enables it to detect evolutionary events in noncoding regions. We demonstrate using simulated data that DivE compares favorably to alternative methods, and we then apply DivE to the ENCODE regions in 14 primate species. We identify thousands of regions in these primates, ranging from 50 to >10000 bp in length, that appear to have experienced either constrained or accelerated rates of evolution. In particular, we detected 4942 regions that have potentially undergone positive selection in one or more primate species. Most of these regions occur outside of protein-coding genes, although we identified 20 proteins that have experienced positive selection.DivE provides an easy-to-use method to predict both positive and negative selection in noncoding DNA, that is particularly well-suited to detecting lineage-specific selection in large genomes.
| S-EPMC3143108 | biostudies-literature
Project description:Rabbitfish (Siganidae) are coral reef fish that are distributed across diverse habitats that include estuaries, mangroves, reefs, and even seaweed mats. Given their ecological diversity and natural widespread distributions across the Indo-Pacific region, we were interested to investigate the evolutionary history of this group and patterns of divergence that have contributed to their present-day distributions. In the present study, samples were collected from the South China Sea to study taxonomic and phylogenetic relationships, and divergence times. We investigated the taxonomic relationships among modern rabbitfish species, reconstructed their molecular phylogeny, and estimated divergence times among selected lineages based on a fragment of the mtDNA cytochrome oxidase I (COI) and sequences of the nuclear rhodopsin retrogene (RHO). Our results indicate that modern rabbitfish likely originated in the Indo-West Pacific during the late Eocene [37.4 million years ago (mya)], following which they diverged into three major clades during the Pliocene/Pleistocene. Subsequent diversification and origins of the majority of siganids may likely be associated with episodes of paleo-oceanographic events, including greenhouse and glaciation events (Eocene-Miocene) as well as major plate tectonic events (Pliocene-Pleistocene). Some modern siganid species may naturally hybridize with congeneric species where their geographical ranges overlap. A comprehensive taxonomic analysis revealed that the phylogeny of Siganidae (cladogenesis of Clades I, II, and III) is characterized by divergence in several external morphological characters and morphometric parameters. Our study demonstrates that morphological characteristics, geographical heterogeneity, and environmental change have contributed to siganids' historical diversification.
| S-EPMC8615046 | biostudies-literature
Project description:Without the sustained provision of adequate levels of oxygen by the cardiovascular system, the tissues of higher animals are incapable of maintaining normal metabolic activity, and hence cannot survive. The consequence of this evolutionarily suboptimal design is that humans are dependent on cardiovascular perfusion, and therefore highly susceptible to alterations in its normal function. However, hope may be at hand. "Photosynthetic strategies," based on the recognition that photosynthesis is the source of all oxygen, offer a revolutionary and promising solution to pathologies related to tissue hypoxia. These approaches, which have been under development over the past 20 years, seek to harness photosynthetic microorganisms as a local and controllable source of oxygen to circumvent the need for blood perfusion to sustain tissue survival. To date, their applications extend from the in vitro creation of artificial human tissues to the photosynthetic maintenance of oxygen-deprived organs both in vivo and ex vivo, while their potential use in other medical approaches has just begun to be explored. This review provides an overview of the state of the art of photosynthetic technologies and its innovative applications, as well as an expert assessment of the major challenges and how they can be addressed.
| S-EPMC7573207 | biostudies-literature
Project description:Premise of the studyPredictable chloroplast DNA (cpDNA) sequences have been listed for the shallowest taxonomic studies in plants. We investigated whether plastid regions that vary between closely allied species could be applied for intraspecific studies and compared the variation of these plastid segments with two nuclear regions.MethodsWe screened 16 plastid and two nuclear intronic regions for species of the genus Cereus (Cactaceae) at three hierarchical levels (species from different clades, species of the same clade, and allopatric populations).ResultsTen plastid regions presented interspecific variation, and six of them showed variation at the intraspecific level. The two nuclear regions showed both inter- and intraspecific variation, and in general they showed higher levels of variability in almost all hierarchical levels than the plastid segments.DiscussionOur data suggest no correspondence between variation of plastid regions at the interspecific and intraspecific level, probably due to lineage-specific variation in cpDNA, which appears to have less effect in nuclear data. Despite the heterogeneity in evolutionary rates of cpDNA, we highlight three plastid segments that may be considered in initial screenings in plant phylogeographic studies.
| S-EPMC4716776 | biostudies-literature
Project description:The evolutionary success of reef-building corals is often attributed to photosymbiosis, a mutualistic relationship scleractinian corals developed with zooxanthellae; however, because zooxanthellae are not fossilized, it is difficult (and contentious) to determine whether ancient corals harbored symbionts. In this study, we analyze the δ15N of skeletal organic matrix in a suite of modern and fossil scleractinian corals (zooxanthellate- and azooxanthellate-like) with varying levels of diagenetic alteration. Significantly, we report the first analyses that distinguish shallow-water zooxanthellate and deep-water azooxanthellate fossil corals. Early Miocene (18-20 Ma) corals exhibit the same nitrogen isotopic ratio offset identified in modern corals. These results suggest that the coral organic matrix δ15N proxy can successfully be used to detect photosymbiosis in the fossil record. This proxy will significantly improve our ability to effectively define the evolutionary relationship between photosymbiosis and reef-building through space and time. For example, Late Triassic corals have symbiotic values, which tie photosymbiosis to major coral reef expansion. Furthermore, the early Miocene corals from Indonesia have low δ15N values relative to modern corals, implying that the west Pacific was a nutrient-depleted environment and that oligotrophy may have facilitated the diversification of the reef builders in the Coral Triangle.
| S-EPMC5572714 | biostudies-literature
Project description:This review explores how microbial symbioses may have influenced and continue to influence the evolution of reef-building corals (Cnidaria; Scleractinia). The coral holobiont comprises a diverse microbiome including dinoflagellate algae (Dinophyceae; Symbiodiniaceae), bacteria, archaea, fungi and viruses, but here we focus on the Symbiodiniaceae as knowledge of the impact of other microbial symbionts on coral evolution is scant. Symbiosis with Symbiodiniaceae has extended the coral's metabolic capacity through metabolic handoffs and horizontal gene transfer (HGT) and has contributed to the ecological success of these iconic organisms. It necessitated the prior existence or the evolution of a series of adaptations of the host to attract and select the right symbionts, to provide them with a suitable environment and to remove disfunctional symbionts. Signatures of microbial symbiosis in the coral genome include HGT from Symbiodiniaceae and bacteria, gene family expansions, and a broad repertoire of oxidative stress response and innate immunity genes. Symbiosis with Symbiodiniaceae has permitted corals to occupy oligotrophic waters as the algae provide most corals with the majority of their nutrition. However, the coral-Symbiodiniaceae symbiosis is sensitive to climate warming, which disrupts this intimate relationship, causing coral bleaching, mortality and a worldwide decline of coral reefs. This article is part of the theme issue 'The role of the microbiome in host evolution'.
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Project description:Starch is the most widespread and abundant storage carbohydrate in plants. It is also a major feature of cultivated bananas as it accumulates to large amounts during banana fruit development before almost complete conversion to soluble sugars during ripening. Little is known about the structure of major gene families involved in banana starch metabolism and their evolution compared to other species. To identify genes involved in banana starch metabolism and investigate their evolutionary history, we analyzed six gene families playing a crucial role in plant starch biosynthesis and degradation: the ADP-glucose pyrophosphorylases (AGPases), starch synthases (SS), starch branching enzymes (SBE), debranching enzymes (DBE), α-amylases (AMY) and β-amylases (BAM). Using comparative genomics and phylogenetic approaches, these genes were classified into families and sub-families and orthology relationships with functional genes in Eudicots and in grasses were identified. In addition to known ancestral duplications shaping starch metabolism gene families, independent evolution in banana and grasses also occurred through lineage-specific whole genome duplications for specific sub-families of AGPase, SS, SBE, and BAM genes; and through gene-scale duplications for AMY genes. In particular, banana lineage duplications yielded a set of AGPase, SBE and BAM genes that were highly or specifically expressed in banana fruits. Gene expression analysis highlighted a complex transcriptional reprogramming of starch metabolism genes during ripening of banana fruits. A differential regulation of expression between banana gene duplicates was identified for SBE and BAM genes, suggesting that part of starch metabolism regulation in the fruit evolved in the banana lineage.
| S-EPMC5133247 | biostudies-literature
Project description:The ability to segregate a committed germ stem cell (GSC) lineage distinct from somatic cell lineages is a characteristic of bilaterian Metazoans. However, the occurrence of GSC lineage specification in basally branching Metazoan phyla, such as Cnidaria, is uncertain. Without an independently segregated GSC lineage, germ cells and their precursors must be specified throughout adulthood from continuously dividing somatic stem cells, generating the risk of propagating somatic mutations within the individual and its gametes. To address the potential for existence of a GSC lineage in Anthozoa, the sister-group to all remaining Cnidaria, we identified moderate- to high-frequency somatic mutations and their potential for gametic transfer in the long-lived coral Orbicella faveolata (Anthozoa, Cnidaria) using a 2b-RAD sequencing approach. Our results demonstrate that somatic mutations can drift to high frequencies (up to 50%) and can also generate substantial intracolonial genetic diversity. However, these somatic mutations are not transferable to gametes, signifying the potential for an independently segregated GSC lineage in O. faveolata. In conjunction with previous research on germ cell development in other basally branching Metazoan species, our results suggest that the GSC system may be a Eumetazoan characteristic that evolved in association with the emergence of greater complexity in animal body plan organization and greater specificity of stem cell functions.
| S-EPMC4721087 | biostudies-literature