The hologenome theory of evolution (HTE), which is under fierce debate, presupposes that parts of the microbiome are transmitted from one generation to the next [vertical transmission (VT)], which may also influence the evolution of the holobiont. Even though bacteria have previously been described in early life stages of corals, these early life stages (larvae) could have been inoculated in the water and not inside the parental colony (through gametes) carrying the parental microbiome. How Symbiodinium is transmitted to offspring is also not clear, as only one study has described this mechanism in spawners. All other studies refer to incubators. To explore the VT hypothesis and the key components being transferred, colonies of the broadcast spawner species Mussismilia hispida were kept in nurseries until spawning. Gamete bundles, larvae and adult corals were analyzed to identify their associated microbiota with respect to composition and location. Symbiodinium and bacteria were detected by sequencing in gametes and coral planula larvae. However, no cells were detected using microscopy at the gamete stage, which could be related to the absence of those cells inside the oocytes/dispersed in the mucus or to a low resolution of our approach. A preliminary survey of Symbiodinium diversity indicated that parental colonies harbored Symbiodinium clades B, C and G, whereas only clade B was found in oocytes and planula larvae [5 days after fertilization (a.f.)]. The core bacterial populations found in the bundles, planula larvae and parental colonies were identified as members of the genera Burkholderia, Pseudomonas, Acinetobacter, Ralstonia, Inquilinus and Bacillus, suggesting that these populations could be vertically transferred through the mucus. The collective data suggest that spawner corals, such as M. hispida, can transmit Symbiodinium cells and the bacterial core to their offspring by a coral gamete (and that this gamete, with its bacterial load, is released into the water), supporting the HTE. However, more data are required to indicate the stability of the transmitted populations to indicate whether the holobiont can be considered a unit of natural selection or a symbiotic assemblage of independently evolving organisms.
Mass coral bleaching has increased in intensity and frequency and has severely impacted shallow tropical reefs worldwide. Although extensive investigation has been conducted on the resistance and resilience of coral reefs in the Indo-Pacific and Caribbean, the unique reefs of the South Atlantic remain largely unassessed. Here we compiled primary and literature data for reefs from three biogeographical regions: Indo-Pacific, Caribbean and South Atlantic and performed comparative analyses to investigate whether the latter may be more resistant to bleaching. Our findings show that South Atlantic corals display critical features that make them less susceptible to mass coral bleaching: (i) deeper bathymetric distribution, as species have a mean maximum depth of occurrence of 70 m; (ii) higher tolerance to turbidity, as nearly 60% of species are found in turbid conditions; (iii) higher tolerance to nutrient enrichment, as nitrate concentration in the South Atlantic is naturally elevated; (iv) higher morphological resistance, as massive growth forms are dominant and comprise two thirds of species; and (v) more flexible symbiotic associations, as 75% of corals and 60% of symbiont phylotypes are generalists. Such features were associated with occurrence of fewer bleaching episodes with coral mortality in the South Atlantic, approximately 60% less than the Indo-Pacific and 50% less than the Caribbean. In addition, no mass coral mortality episodes associated with the three global mass bleaching events have been reported for the South Atlantic, which suffered considerably less bleaching. These results show that South Atlantic reefs display several remarkable features for withstanding thermal stress. Together with a historic experience of lower heat stress, our findings may explain why climate change impacts in this region have been less intense. Given the large extension and latitudinal distribution of South Atlantic coral reefs and communities, the region may be recognized as a major refugium and likely to resist climate change impacts more effectively than Indo-Pacific and Caribbean reefs.
Threatened by global warming and extreme climatic events, such as El Niño Southern Oscillation (ENSO) and Marine Heatwaves (MHW), coral reefs worldwide faced the worst bleaching and mortality event between 2014 and 2017, induced by the 2015/2016 ENSO. We evaluated the impacts of ENSO and MHW episodes on bleaching and mortality frequencies of Siderastrea stellata at Rocas Atoll, Southwestern Atlantic, using visual censuses conducted in 2016, 2017 and 2019. Bleaching rate varied significantly along the sampling period (11.71% in 2016, 1.52% in 2017, and 88% in 2019), but mortality was always less than 4%. Bleaching events in Atlantic reefs have been constantly associated with ENSO, until these recent events of the last two years. We suggest that MHW were probably the primary driver of the observed bleaching, especially in 2019, when much higher bleaching rates were observed than in ENSO periods. Although Southwestern Atlantic massive corals are considered more resistant to thermal stress than reefs corals worldwide, the strong events registered since 2019 highlight the need for continuous monitoring to better understand coral bleaching dynamics and improve predictions on the effects of global change in the region.
Zooxanthellate corals live in symbiosis with phototrophic dinoflagellates of the family Symbiodiniaceae, enabling the host coral to dwell in shallow, nutrient-poor marine waters. The South Atlantic Ocean is characterized by low coral diversity with high levels of endemism. However, little is known about coral–dinoflagellate associations in the region. This study examined the diversity of Symbiodiniaceae associated with the scleractinian coral Favia gravida across its distributional range using the ITS-2 marker. This brooding coral endemic to the South Atlantic can be found across a wide range of latitudes and longitudes, including the Mid-Atlantic islands. Even though it occurs primarily in shallower environments, F . gravida is among the few coral species that live in habitats with extreme environmental conditions (high irradiance, temperature, and turbidity) such as very shallow tide pools. In the present study, we show that F . gravida exhibits some degree of flexibility in its symbiotic association with zooxanthellae across its range. F . gravida associates predominantly with Cladocopium C3 (ITS2 type Symbiodinium C3) but also with Symbiodinium A3, Symbiodinium linucheae (ITS2 type A4), Cladocopium C1, Cladocopium C130, and Fugacium F3. Symbiont diversity varied across biogeographic regions ( Symbiodinium A3 and S . linucheae were found in the Tropical Eastern Atlantic, Cladocopium C1 in the Mid-Atlantic, and other subtypes in the Southwestern Atlantic) and was affected by local environmental conditions. In addition, Symbiodiniaceae diversity was highest in a southwestern Atlantic oceanic island (Rocas Atoll). Understanding the relationship between corals and their algal symbionts is critical in determining the factors that control the ecological niches of zooxanthellate corals and their symbionts, and identifying host-symbiont pairs that may be more resistant to environmental changes.
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