Background: Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. A novel group of apicomplexans, recently named corallicolids, have been detected in corals inhabiting tropical shallow reefs. These apicomplexans may represent a transitional lifestyle between free-living phototrophs and obligate parasites. To shed light on the evolutionary history of apicomplexans and to investigate their ecology in association with corals, we screened scleractinians, antipatharians, alcyonaceans, and zoantharians from shallow, mesophotic, and deep-sea communities. We detected corallicolid plastids using 16S metabarcoding, sequenced the nuclear 18S rRNA gene of corallicolids from selected samples, assembled and annotated the plastid and mitochondrial genomes from a corallicolid that associates with a deep-sea coral, and screened the metagenomes of four coral species for corallicolids. Results: We detected 23 corallicolid plastotypes that were associated with 14 coral species from three orders and depths down to 1400 m. Individual plastotypes were restricted to coral hosts within a single depth zone and within a single taxonomic order of corals. Some clusters of closely related corallicolids were revealed that associated with closely related coral species. However, the presence of divergent corallicolid lineages that associated with similar coral species and depths suggests that corallicolid/coral relations are flexible over evolutionary timescales and that a large diversity of apicomplexans may remain undiscovered. The corallicolid plastid genome from a deep-sea coral contained four genes involved in chlorophyll biosynthesis: the three genes of the LIPOR complex and acsF. Conclusions: The presence of corallicolid apicomplexans in corals below the photic zone demonstrates that they are not restricted to shallow-water reefs and are more general anthozoan symbionts. The presence of LIPOR genes in the deep-sea corallicolid precludes a role involving photosynthesis and suggests they may be involved in a different function. Thus, these genes may represent another set of genetic tools whose function was adapted from photosynthesis as the ancestors of apicomplexans evolved towards parasitic lifestyles.
Environmental DNA (eDNA) quantification and sequencing are emerging techniques for assessing biodiversity in marine ecosystems. Environmental DNA can be transported by ocean currents and may remain at detectable concentrations far from its source depending on how long it persist. Thus, predicting the persistence time of eDNA is crucial to defining the spatial context of the information derived from it. To investigate the physicochemical controls of eDNA persistence, we performed degradation experiments at temperature, pH, and oxygen conditions relevant to the open ocean and the deep sea. The eDNA degradation process was best explained by a model with two phases with different decay rate constants. During the initial phase, eDNA degraded rapidly, and the rate was independent of physicochemical factors. During the second phase, eDNA degraded slowly, and the rate was strongly controlled by temperature, weakly controlled by pH, and not controlled by dissolved oxygen concentration. We demonstrate that marine eDNA can persist at quantifiable concentrations for over 2 weeks at low temperatures (≤10 °C) but for a week or less at ≥20 °C. The relationship between temperature and eDNA persistence is independent of the source species. We propose a general temperature-dependent model to predict the maximum persistence time of eDNA detectable through single-species eDNA quantification methods.
Introduction From shallow water to the deep sea, corals form the basis of diverse communities with significant ecological and economic value. These communities face many anthropogenic stressors including energy and mineral extraction activities, ocean acidification and rising sea temperatures. Corals and their symbionts produce a diverse assemblage of compounds that may help provide resilience to some of these stressors. Objectives We aim to characterize the metabolomic diversity of deep-sea corals in an ecological context by investigating patterns across space and phylogeny. Methods We applied untargeted Liquid Chromatography-Mass Spectrometry to examine the metabolomic diversity of the deep-sea coral, Callogorgia delta , across three sites in the Northern Gulf of Mexico as well as three other deep-sea corals, Stichopathes sp., Leiopathes glaberrima , and Lophelia pertusa , and a shallow-water species, Acropora palmata . Results Different coral species exhibited distinct metabolomic fingerprints and differences in metabolomic richness including core ions unique to each species. C. delta was generally least diverse while Lophelia pertusa was most diverse. C. delta from different sites had different metabolomic fingerprints and metabolomic richness at individual and population levels, although no sites exhibited unique core ions. Two core ions unique to C. delta were putatively identified as diterpenes and thus may possess a biologically important function. Conclusion Deep-sea coral species have distinct metabolomic fingerprints and exhibit high metabolomic diversity at multiple scales which may contribute to their capabilities to respond to both natural and anthropogenic stressors, including climate change. Electronic supplementary material The online version of this article (10.1007/s11306-019-1500-y) contains supplementary material, which is available to authorized users.
Since 1892, it has been widely assumed that somatic mutations are evolutionarily irrelevant in animals because they cannot be inherited by offspring. However, some nonbilaterians segregate the soma and germline late in development or never, leaving the evolutionary fate of their somatic mutations unknown. By investigating uni- and biparental reproduction in the coral Acropora palmata (Cnidaria, Anthozoa), we found that uniparental, meiotic offspring harbored 50% of the 268 somatic mutations present in their parent. Thus, somatic mutations accumulated in adult coral animals, entered the germline, and were passed on to swimming larvae that grew into healthy juvenile corals. In this way, somatic mutations can increase allelic diversity and facilitate adaptation across habitats and generations in animals.
8Cnidarians are known for their symbiotic relationships, yet no known association exists 9 between corals and chemoautotrophic microbes. Deep-sea corals, which support diverse animal 10 communities in the Gulf of Mexico, are often found on authigenic carbonate in association with 11 cold seeps. Sulfur-oxidizing chemoautotrophic bacteria of the SUP05 cluster are dominant 12 symbionts of bathymodiolin mussels at cold seeps and hydrothermal vents around the world and 13 have also been found in association with sponges. Therefore, we investigated whether other basal 14 metazoans, corals, also associate with bacteria of the SUP05 cluster and report here that such 15 associations are widespread. This was unexpected because it has been proposed that cnidarians 16 would not form symbioses with chemoautotrophic bacteria due to their high oxygen demand and 17 their lack of specialized respiratory structures. We screened corals, water, and sediment for 18 SUP05 using 16S metabarcoding and found SUP05 phylotypes associated with corals at high 19 relative abundance (10 -91%). These coral-associated SUP05 phylotypes were coral host 20 specific, absent in water samples, and rare or not detected in sediment samples. The genome of 21 one SUP05 phylotype associated with Paramuricea sp. type B3, contained the genetic potential 22 to oxidize reduced sulfur compounds and fix carbon and these pathways were transcriptionally 23 active. Finally, the relative abundance of this SUP05 phylotype was positively correlated with 24 2 chemoautotrophically-derived carbon and nitrogen input into the coral holobiont based on stable 25 carbon and nitrogen isotopic compositions. We propose that SUP05 may supplement the diet of 26 its host coral through chemoautotrophy or may provide nitrogen, essential amino acids, or 27 vitamins. This is the first documented association between a chemoautotrophic symbiont and a 28 cnidarian, broadening the known symbioses of corals and may represent a novel interaction 29 between coral communities and cold seeps. 30
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