Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis.
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ABSTRACT:
SUBMITTER: Liu H
PROVIDER: S-EPMC6123633 | biostudies-literature | 2018
REPOSITORIES: biostudies-literature
Publications
<i>Symbiodinium</i> genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis.
Liu Huanle H Stephens Timothy G TG González-Pech Raúl A RA Beltran Victor H VH Lapeyre Bruno B Bongaerts Pim P Cooke Ira I Aranda Manuel M Bourne David G DG Forêt Sylvain S Miller David J DJ van Oppen Madeleine J H MJH Voolstra Christian R CR Ragan Mark A MA Chan Cheong Xin CX
Communications biology 20180717
Symbiosis between dinoflagellates of the genus <i>Symbiodinium</i> and reef-building corals forms the trophic foundation of the world's coral reef ecosystems. Here we present the first draft genome of <i>Symbiodinium goreaui</i> (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of <i>Symbiodinium kawagutii</i> (Clade F, strain CS-156: 1.05 Gbp) to further elucidate genomic signatures of this symbiosis. Comparative analysis ...[more]
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Project description:Coral reefs are some of the most diverse and productive ecosystems on the planet, but are threatened by global and local stressors, mandating the need for incorporating ex situ conservation practices. One approach that is highly protective is the development of genome resource banks that preserve the species and its genetic diversity. A critical component of the reef are the endosymbiotic algae, Symbiodinium sp., living within most coral that transfer energy-rich sugars to their hosts. Although Symbiodinium are maintained alive in culture collections around the world, the cryopreservation of these algae to prevent loss and genetic drift is not well-defined. This study examined the quantum yield physiology and freezing protocols that resulted in survival of Symbiodinium at 24 h post-thawing. Only the ultra-rapid procedure called vitrification resulted in success whereas conventional slow freezing protocols did not. We determined that success also depended on using a thin film of agar with embedded Symbiodinium on Cryotops, a process that yielded a post-thaw viability of >50% in extracted and vitrified Symbiodinium from Fungia scutaria, Pocillopora damicornis and Porites compressa. Additionally, there also was a seasonal influence on vitrification success as the best post-thaw survival of F. scutaria occurred in winter and spring compared to summer and fall (P < 0.05). These findings lay the foundation for developing a viable genome resource bank for the world's Symbiodinium that, in turn, will not only protect this critical element of coral functionality but serve as a resource for understanding the complexities of symbiosis, support selective breeding experiments to develop more thermally resilient strains of coral, and provide a 'gold-standard' genomics collection, allowing for full genomic sequencing of unique Symbiodinium strains.
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Project description:Many aspects of an individual's biology derive from its interaction with symbiotic microbes, which further define many aspects of the ecology and evolution of the host species. The centrality of microbes in the function of individual organisms has given rise to the concept of the holobiont-that an individual's biology is best understood as a composite of the 'host organism' and symbionts within. This concept has been further elaborated to posit the holobiont as a unit of selection. In this review, I critically examine whether it is useful to consider holobionts as a unit of selection. I argue that microbial heredity-the direct passage of microbes from parent to offspring-is a key factor determining the degree to which the holobiont can usefully be considered a level of selection. Where direct vertical transmission (VT) is common, microbes form part of extended genomes whose dynamics can be modelled with simple population genetics, but that nevertheless have subtle quantitative distinctions from the classic mutation/selection model for nuclear genes. Without direct VT, the correlation between microbial fitness and host individual fitness erodes, and microbe fitness becomes associated with host survival only (rather than reproduction). Furthermore, turnover of microbes within a host may lessen associations between microbial fitness with host survival, and in polymicrobial communities, microbial fitness may derive largely from the ability to outcompete other microbes, to avoid host immune clearance and to minimize mortality through phage infection. These competing selection pressures make holobiont fitness a very minor consideration in determining symbiont evolution. Nevertheless, the importance of non-heritable microbes in organismal function is undoubted-and as such the evolutionary and ecological processes giving rise to variation and evolution of the microbes within and between host individuals represent a key research area in biology.
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Project description:Many reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. There is increasing evidence of functional significance to Symbiodinium diversity, which affects the coral holobiont's response to changing environmental conditions. For example, corals hosting Symbiodinium from the clade D taxon exhibit greater resistance to heat-induced coral bleaching than conspecifics hosting the more common clade C. Yet, the relatively low prevalence of clade D suggests that this trait is not advantageous in non-stressful environments. Thus, clade D may only be able to out-compete other Symbiodinium types within the host habitat when conditions are chronically stressful. Previous studies have observed enhanced photosynthesis and fitness by clade C holobionts at non-stressful temperatures, relative to clade D. Yet, carbon-centered metrics cannot account for enhanced growth rates and patterns of symbiont succession to other genetic types when nitrogen often limits reef productivity. To investigate the metabolic costs of hosting thermally tolerant symbionts, we examined the assimilation and translocation of inorganic (15)N and (13)C in the coral Acropora tenuis experimentally infected with either clade C (sub-type C1) or D Symbiodinium at 28 and 30 °C. We show that at 28 °C, C1 holobionts acquired 22% more (15)N than clade D. However, at 30 °C, C1 symbionts acquired equivalent nitrogen and 16% less carbon than D. We hypothesize that C1 competitively excludes clade D in hospite via enhanced nitrogen acquisition and thus dominates coral populations despite warming oceans.
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Project description:Symbiodinium is best-known as the photosynthetic symbiont of corals, but some clades are symbiotic in other organisms or include free-living forms. Identifying similarities and differences among these clades can help us understand their relationship with corals, and thereby inform on measures to manage coral reefs in a changing environment. Here, using sequences from 24 publicly available transcriptomes and genomes of Symbiodinium, we assessed 78,389 gene families in Symbiodinium clades and the immediate outgroup Polarella glacialis, and identified putative overrepresented functions in gene families that (1) distinguish Symbiodinium from other members of Order Suessiales, (2) are shared by all of the Symbiodinium clades for which we have data, and (3) based on available information, are specific to each clade. Our findings indicate that transmembrane transport, mechanisms of response to reactive oxygen species, and protection against UV radiation are functions enriched in all Symbiodinium clades but not in P. glacialis. Enrichment of these functions indicates the capability of Symbiodinium to establish and maintain symbiosis, and to respond and adapt to its environment. The observed differences in lineage-specific gene families imply extensive genetic divergence among clades. Our results provide a platform for future investigation of lineage- or clade-specific adaptation of Symbiodinium to their environment.
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Project description:Assimilation of inorganic nitrogen from nutrient-poor tropical seas is an essential challenge for the endosymbiosis between reef-building corals and dinoflagellates. Despite the clear evidence that reef-building corals can use ammonium as inorganic nitrogen source, the dynamics and precise roles of host and symbionts in this fundamental process remain unclear. Here, we combine high spatial resolution ion microprobe imaging (NanoSIMS) and pulse-chase isotopic labeling in order to track the dynamics of ammonium incorporation within the intact symbiosis between the reef-building coral Acropora aspera and its dinoflagellate symbionts. We demonstrate that both dinoflagellate and animal cells have the capacity to rapidly fix nitrogen from seawater enriched in ammonium (in less than one hour). Further, by establishing the relative strengths of the capability to assimilate nitrogen for each cell compartment, we infer that dinoflagellate symbionts can fix 14 to 23 times more nitrogen than their coral host cells in response to a sudden pulse of ammonium-enriched seawater. Given the importance of nitrogen in cell maintenance, growth and functioning, the capability to fix ammonium from seawater into the symbiotic system may be a key component of coral nutrition. Interestingly, this metabolic response appears to be triggered rapidly by episodic nitrogen availability. The methods and results presented in this study open up for the exploration of dynamics and spatial patterns associated with metabolic activities and nutritional interactions in a multitude of organisms that live in symbiotic relationships.
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Project description:BackgroundIntegrating demography and adaptive evolution is pivotal to understanding the evolutionary history and conservation of great apes. However, little is known about the adaptive evolution of our closest relatives, in particular if and to what extent adaptions to environmental differences have occurred. Here, we used whole-genome sequencing data from critically endangered orangutans from North Sumatra (Pongo abelii) and Borneo (P. pygmaeus) to investigate adaptive responses of each species to environmental differences during the Pleistocene.ResultsTaking into account the markedly disparate demographic histories of each species after their split ~ 1 Ma ago, we show that persistent environmental differences on each island had a strong impact on the adaptive evolution of the genus Pongo. Across a range of tests for positive selection, we find a consistent pattern of between-island and species differences. In the more productive Sumatran environment, the most notable signals of positive selection involve genes linked to brain and neuronal development, learning, and glucose metabolism. On Borneo, however, positive selection comprised genes involved in lipid metabolism, as well as cardiac and muscle activities.ConclusionsWe find strikingly different sets of genes appearing to have evolved under strong positive selection in each species. In Sumatran orangutans, selection patterns were congruent with well-documented cognitive and behavioral differences between the species, such as a larger and more complex cultural repertoire and higher degrees of sociality. However, in Bornean orangutans, selective responses to fluctuating environmental conditions appear to have produced physiological adaptations to generally lower and temporally more unpredictable food supplies.
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Project description:Symbiodinium, a large group of dinoflagellates, live in symbiosis with marine protists, invertebrate metazoans, and free-living in the environment. Symbiodinium are functionally variable and play critical energetic roles in symbiosis. Our knowledge of Symbiodinium has been historically constrained by the limited number of molecular markers available to study evolution in the genus. Here we compare six functional genes, representing three cellular compartments, in the nine known Symbiodinium lineages. Despite striking similarities among the single gene phylogenies from distinct organelles, none were evolutionarily identical. A fully concatenated reconstruction, however, yielded a well-resolved topology identical to the current benchmark nr28S gene. Evolutionary rates differed among cellular compartments and clades, a pattern largely driven by higher rates of evolution in the chloroplast genes of Symbiodinium clades D2 and I. The rapid rates of evolution observed amongst these relatively uncommon Symbiodinium lineages in the functionally critical chloroplast may translate into potential innovation for the symbiosis. The multi-gene analysis highlights the potential power of assessing genome-wide evolutionary patterns using recent advances in sequencing technology and emphasizes the importance of integrating ecological data with more comprehensive sampling of free-living and symbiotic Symbiodinium in assessing the evolutionary adaptation of this enigmatic dinoflagellate.
| S-EPMC4034598 | biostudies-literature