Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont
Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coral
- PAR ID:
- 10446044
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 31
- Issue:
- 2
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 588-602
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand howD. trenchii modulates coral gene expression by manipulating symbiont communities inMontastraea cavernosa to produce replicate ramets containingD. trenchii together with paired ramets of these same genets (n = 3) containingCladocopium C3 symbionts. We then examined differences in global gene expression between corals hostingDurusdinium andCladocopium under control temperatures, and in response to short‐term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%–14% of the transcriptional variance. Corals withD. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals withCladocopium . Unexpectedly, these changes were similar to those observed inCladocopium‐ dominated corals in response to heat stress, suggesting that thermotolerantD. trenchii may cause corals to increase expression of heat stress‐responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containingD. trenchii . These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts. -
more » « less
Abstract Many 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 a variety of multilocus genotypes (MLG) within two genetically distinctCladocopium lineages (C40, C21), confirming thatAcropora coral hosts associate with a range ofCladocopium symbionts across this region. Both C40 and C21 included multiple asexual lineages bearing identical MLGs, many of which spanned host species, reef sites within islands, and even different islands. Both C40 and C21 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‐associatedCladocopium 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 dispersingAcropora coral species. -
more » « less
Abstract Dinoflagellates are a diverse group of phytoplankton, ranging from harmful bloom-forming microalgae to photosymbionts of coral reefs. Genome-scale data from dinoflagellates reveal atypical genomic features, extensive genomic divergence, and lineage-specific innovation of gene functions. Long non-coding RNAs (lncRNAs), known to regulate gene expression in eukaryotes, are largely unexplored in dinoflagellates. Here, using high-quality genome and transcriptome data, we identified 48039 polyadenylated lncRNAs in three dinoflagellate species: the coral symbionts Cladocopium proliferum and Durusdinium trenchii, and the bloom-forming species, Prorocentrum cordatum. These lncRNAs have fewer introns and lower G+C content than protein-coding sequences; 37 768 (78.6%) are unique with respect to sequence similarity. We classified all lncRNAs based on conserved motifs (k-mers) into distinct clusters, following properties of protein-binding and/or subcellular localisation. Interestingly, 3708 (7.7%) lncRNAs are differentially expressed under heat stress, algal lifestyle, and/or growth phase, and share co-expression patterns with protein-coding genes. Based on inferred triplex interactions between lncRNA and putative promoter regions, we identified 19 460 putative gene targets for 3721 lncRNAs; 907 genes exhibit differential expression under heat stress. These results reveal, for the first time, the diversity of lncRNAs in dinoflagellates and how lncRNAs may regulate gene expression as a heat-stress response in these ecologically important microbes.
-
more » « less
Abstract Individuals often differ in their ability to cope with challenging environmental and social conditions. Evidence from model systems suggests that patterns of DNA methylation are associated with variation in coping ability. These associations could arise directly if methylation plays a role in controlling the physiological response to stressors by, among other things, regulating the release of glucocorticoids in response to challenges. Alternatively, the association could arise indirectly if methylation and resilience have a common cause, such as early‐life conditions. In either case, methylation might act as a biomarker for coping ability. At present, however, relatively little is known about whether variation in methylation is associated with organismal performance and resilience under natural conditions. We studied genome‐wide patterns of DNA methylation in free‐living female tree swallows (
Tachycineta bicolor ) using methylated DNA immunoprecipitation (MeDIP) and a tree swallow genome that was assembled for this study. We identified areas of the genome that were differentially methylated with respect to social signal expression (breast brightness) and physiological traits (ability to terminate the glucocorticoid stress response through negative feedback). We also asked whether methylation predicted resilience to a subsequent experimentally imposed challenge. Individuals with brighter breast plumage and higher stress resilience had lower methylation at differentially methylated regions across the genome. Thus, widespread differences in methylation predicted both social signal expression and the response to future challenges under natural conditions. These results have implications for predicting individual differences in resilience, and for understanding the mechanistic basis of resilience and its environmental and social mediators. -
more » « less
Summary Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we use
Tragopogon (Asteraceae) as a model system to discover patterns and temporal dynamics of DNA methylation in recently formed polyploids.The naturally occurring allotetraploid
Tragopogon miscellus formed in the last 95–100 yr from parental diploidsTragopogon dubius andT. pratensis . We profiled the DNA methylomes of these three species using whole‐genome bisulfite sequencing.Genome‐wide methylation levels in
T. miscellus were intermediate between its diploid parents. However, nonadditive CG and CHG methylation occurred in transposable elements (TEs), with variation among TE types. Most differentially methylated regions (DMRs) showed parental legacy, but some novel DMRs were detected in the polyploid. Differentially methylated genes (DMGs) were also identified and characterized.This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes.
