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Biology subjects

Dixon, G. B.

Publications and source records attributed to Dixon, G. B..

7 recordsLinked to original sources

Symbiosis modulates gene expression of symbionts, but not hosts, under thermal challenge

Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coral Oculina arbuscula and its symbiont Breviolum psygmophilum to characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbiotic O. arbuscula were exposed to three treatments: 1) control (18{degrees}C), 2) heat (32{degrees}C), and 3) cold (6{degrees}C). This experiment was replicated with B. psygmophilum cultured from O. arbuscula to characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) in O. arbuscula regardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospite B. psygmophilum both downregulated genes associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest that O. arbuscula hosts may buffer environments of B. psygmophilum symbionts; however, we outline the future work needed to confirm this hypothesis.

molecular biology↗

Codominance of two symbiont genera within the same coral host is associated with elevated symbiont productivity and lower host susceptibility to thermal stress

In recent years, as sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how the symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this interaction has on the host. We used previously published transcriptomic data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportion of the two symbiont genera within the same host. We find that both Cladocopium and Durusdinium change their expression the most when their proportions within the host are nearly equal (the state that we call "codominance"): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two alternative ways. One explanation is that increased competition between codominant symbionts switches them to the higher productivity mode, which benefits the host, making it more resilient to stress. Alternatively, the symbionts elevated productivity might be not the cause but the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbioints competition and thus promoting their growth, which allows for codominance to happen where one genus would otherwise outcompete another. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities, assessed as relative proportions of symbiont reads in the data. Irrespective of the causation direction, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

evolutionary biology↗

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

Broadcast-spawning coral species have wide geographic ranges, spanning strong environmental gradients, but it is unclear how much spatially varying selection these gradients actually impose. Strong divergent selection might present a considerable barrier for demographic exchange between disparate reef habitats. We investigated whether the cross-shelf gradient (nearshore - offshore - deep) is associated with spatially varying selection in two common coral species, Montastraea cavernosa and Siderastrea siderea, in the Florida Keys. Toward this end, we generated a de novo genome assembly for M. cavernosa and used 2bRAD to genotype 20 juveniles and 20 adults of both species from each of the three reef zones to identify signatures of selection occurring within a single generation. Unexpectedly, each species was found to be composed of four genetically distinct lineages, with gene flow between them still ongoing but highly reduced in 13.0-54.7% of the genome. Each species includes two sympatric lineages that are only found in the deep (20 m) habitat, while the other lineages are found almost exclusively on the shallower reefs (3-10 m). The two "shallow" lineages of M. cavernosa are also specialized for either nearshore or offshore: comparison between adult and juvenile cohorts indicates that cross-shelf migrants are more than twice as likely to die before reaching adulthood than local recruits. Siderastrea siderea and M. cavernosa are among the most ecologically successful species on the degraded Florida Keys Reef Tract, and this work offers important insight on the genomic background of divergent selection and environmental specialization that may in part explain their resilience and broad environmental range.

evolutionary biology↗

Testing the caves-as-islands model in two cave-obligate invertebrates with a genomic approach

Caves offer selective pressures that are distinct from the surface. Organisms that have evolved to exist under these pressures typically exhibit a suite of convergent characteristics, including a loss or reduction of eyes and pigmentation. As a result, cave-obligate taxa, termed troglobionts, are no longer viable on the surface. This circumstance has led to a "caves as islands" model of troglobiont evolution that predicts extreme genetic divergence between cave populations even across relatively small areas. An effective test of this model would involve (1) common troglobionts from (2) nearby caves in a cave-dense region, (3) good sample sizes per cave, (4) multiple taxa, and (5) genome-wide characterization. With these criteria in mind, we used RAD-seq to genotype an average of ten individuals of the troglobiotic spider Nesticus barri and the troglobiotic beetle Ptomaphagus hatchi, each from four closely located caves (ranging from 3-13 km apart) in the cave-rich southern Cumberland Plateau of Tennessee, USA. Consistent with the caves as islands model, we find that populations from separate caves are indeed highly genetically isolated. In addition, nucleotide diversity was correlated to cave length, suggesting that cave size is a dominant force shaping troglobiont population size and genetic diversity. Our results support the idea of caves as natural laboratories for the study of parallel evolutionary processes.

genomics↗

A reduction in convergent extension underlies susceptibility to midfacial hypoplasia in the ethanol-sensitive mutant,

AO_SCPLOWBSTRACTC_SCPLOWGene-environment interactions are likely to underlie most human birth defects. The most common environmental contributor to birth defects is likely prenatal alcohol exposure. Fetal Alcohol Spectrum Disorders (FASD) describes the full range of defects that result from prenatal alcohol exposure. Gene-ethanol interactions underlie susceptibility to FASD but we lack a mechanistic understanding of these interactions. Here, we leverage the genetic tractability of zebrafish to address this problem. We first show that vangl2, a member of the Wnt/planar cell polarity (Wnt/PCP) pathway that mediates convergent extension movements, strongly interacts with ethanol during late blastula and early gastrula stages. Embryos mutant or heterozygous for vangl2 are sensitized to ethanol- induced midfacial hypoplasia. We performed single-embryo RNA-Seq during early embryonic stages, to assess individual variation to the transcriptional response to ethanol and determine the mechanism of the vangl2-ethanol interaction. To identify the pathway(s) that are disrupted by ethanol we used these global changes in gene expression to identify small molecules that mimic the effects of ethanol via the Library of Integrated Network- based Cellular Signatures (LINCS L1000) dataset. Surprisingly, this dataset predicted that the Sonic Hedgehog (Shh) pathway inhibitor, cyclopamine, would mimic the effects of ethanol, despite the fact that ethanol did not alter the expression levels of direct targets of Shh signaling. Indeed, we found that ethanol and cyclopamine strongly interact to disrupt midfacial development. Collectively, these results suggest that the midfacial defects in ethanol-exposed vangl2 mutants are due to an indirect interaction between ethanol and the Shh pathway. Vangl2 functions as part of a signaling pathway that regulates coordinated cell movements during midfacial development. Consistent with an indirect model, a critical source of Shh signaling that separates the developing eye field into bilateral eyes, allowing the expansion of the midface, becomes mispositioned in ethanol-exposed vangl2 mutants. We demonstrate that ethanol also interacts with another Wnt/PCP pathway member, gpc4, and a chemical inhibitor, blebbistatin. By characterizing membrane protrusions, we demonstrate that ethanol synergistically interacts with the loss of vangl2 to disrupt cell polarity required for convergent extension movements. Collectively, our results shed light on the mechanism by which the most common teratogen can disrupt development.

developmental biology↗

Molecular convergence and positive selection associated with the evolution of symbiont transmission mode in stony corals

Heritable symbioses are thought to be important for the maintenance of mutually beneficial relationships (1), and for facilitating major transitions in individuality, such as the evolution of the eukaryotic cell (2, 3). In stony corals, vertical transmission has evolved repeatedly (4), providing a unique opportunity to investigate the genomic basis of this complex trait. We conducted a comparative analysis of 25 coral transcriptomes to identify orthologous genes exhibiting both signatures of positive selection and convergent amino acid substitutions in vertically transmitting lineages. The frequency of convergence events tends to be higher among vertically transmitting lineages, consistent with the proposed role of natural selection in driving the evolution of convergent transmission mode phenotypes (5). Of the 10,774 total orthologous genes identified, 403 exhibited at least one molecular convergence event and evidence of positive selection in at least one vertically transmitting lineage. Functional enrichments among these top candidate genes include processes previously implicated in mediating the coral-Symbiodiniaceae symbiosis including endocytosis, immune response, cytoskeletal protein binding and cytoplasmic membrane-bounded vesicles (6). We also identified 100 genes showing evidence of positive selection at the particular convergence event. Among these, we identified several novel candidate genes, highlighting the value of our approach for generating new insight into the mechanistic basis of the coral symbiosis, in addition to uncovering host mechanisms associated with the evolution of heritable symbioses.\n\nDATA ARCHIVAL LOCATIONRaw sequencing data generated for this study have been uploaded to NCBIs SRA: PRJNA395352. All bioinformatic scripts and input files can be found at https://github.com/grovesdixon/convergent_evo_coral.

evolutionary biology↗

Patterns of gene body methylation predict coral fitness in new environments

Despite widespread taxonomic representation, the function of gene body methylation (GBM) remains uncertain. One hypothesis is that GBM mediates phenotypic plasticity. To investigate this hypothesis, we performed whole-genome methylation and transcriptome profiling on reciprocally transplanted colony fragments of the reef-building coral Acropora millepora. GBM was only slightly affected by transplantation but these small changes correlated with coral fitness in the new environment. Specifically, for transplanted corals, similarity in GBM patterns to native corals positively correlated with growth rate, as well as carbohydrate, protein, lipid and endosymbiont content. Between populations, elevated GBM positively correlated with transcription, supporting previous findings that GBM is associated with stable and active transcription. Contrary to expectations however, changes in transcription as a result of transplantation did not correlate with changes in GBM and did not predict fitness. This indicates that on physiological time scales GBM is not directly coupled to transcription, leaving open the question about the mechanism linking GBM to fitness during acclimatization.

ecology↗