Millennia‐old coral holobiont DNA provides insight into future adaptive trajectories

Abstract

Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we utilized aDNA from millennia‐old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE to 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence aDNA from reef cores and place the data in the context of modern‐day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome‐assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern‐day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole‐genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof‐of‐principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.

Decrypting corals: Does regulatory evolution underlie environmental specialization of coral cryptic lineages?

“…Siderastrea siderea reads were cleaned and demultiplexed following the de novo walkthrough (https://github.com/z0on/2bRAD_denovo/blob/master/2bRAD_README.sh). Because there is no genome for S. siderea , reads were first mapped to concatenated Symbiodiniaceae genomes (Dougan et al, 2022; Scott et al, 2022; Shoguchi et al, 2013, 2018) with bowtie2 version 2.4.5 (Langmead & Salzberg, 2012). Any mapped reads were discarded to remove symbiont contamination from coral host reads.…”

“…To determine if the lineages previously described in Rippe et al (2021) were present at the second transect, 2bRAD raw sequences were processed following the same methods described in Rippe et al (2021) (Dougan et al, 2022;Scott et al, 2022;Shoguchi et al, 2013Shoguchi et al, , 2018 with bowtie2 version 2.4.5 (Langmead & Salzberg, 2012). Any mapped reads were discarded to remove symbiont contamination from coral host reads.…”

Paleomicrobiology: Tracking the past microbial life from single species to entire microbial communities

“…As in the case of dental calculus, mineralized structures are however more likely to preserve DNA for longer periods. Thus, Scott et al (2022) successfully extracted and sequenced DNA from millennia-old corals that revealed their original microbiomes which showed similarities to those from today. However, they identified very few sequences that could be affiliated to Symbiodiniaceae, which are essential eukaryotic phototrophic symbionts of corals.…”

Conservation Mitonuclear Replacement: Facilitated mitochondrial adaptation for a changing world

“…+ , 2017;Rogaev et al, 2006;Scott et al, 2022) and can lead to synthetic mtDNA plasmids that may be able to be injected for uptake by recipient mt populations (Gibson et al, 2010;Silva-Pinheiro & Minczuk, 2022). Native recipient mtDNAs could then be targeted for degradation (Jackson et al, 2020;Silva-Pinheiro & Minczuk, 2022; see Appendix S1).…”

“…Extinct haplotypes could replace extant ones with high mutational load, or simply provide more potentially‐adaptive variation on which selection can act. Recovery of ancient mtDNA sequences is possible from frozen remains, specimens, or continuous deposits (Anmarkrud & Lifjeld, 2017 ; Rogaev et al., 2006 ; Scott et al., 2022 ) and can lead to synthetic mtDNA plasmids that may be able to be injected for uptake by recipient mt populations (Gibson et al., 2010 ; Silva‐Pinheiro & Minczuk, 2022 ). Native recipient mtDNAs could then be targeted for degradation (Jackson et al., 2020 ; Silva‐Pinheiro & Minczuk, 2022 ; see Appendix S1 ).…”