Temporal and spatial dynamics of coral symbiont assemblages are affected by local and global impacts.

The influence of abiotic variables and anthropogenic pressure on symbiodiniaceans associated with the scleractinian corals Mussismilia hispida and Siderastrea stellata were assessed quarterly at Armação dos Búzios, Brazil, for over 18 months. Thirty-eight Symbiodiniaceae ITS2 rDNA phylotypes were found by metabarcoding, with eight comprising new phylotypes. Both hosts maintained their generalist pattern, with 1-3 dominant lineages. An environmental pressure index and changes in seawater temperature explained the variations in the structure and diversity of Symbiodiniaceae assemblages over time and space. A mild bleaching event affected the photosymbiotic assemblage structure, even in non-bleached colonies. The highly dynamic and diverse photosymbiont assemblages were constantly driven by the influence of environmental variables and human-induced impacts. Furthermore, new strains of Symbiodiniaceae might be associated with lower temperatures caused by upwelling, which is characteristic of this subtropical coral community, highlighting the region's idiosyncrasy and the need for further studies of this coral system.

How long have we been mistaken? Multi-tools shedding light into the systematics of the widespread deep-water genus Madrepora Linnaeus, 1758 (Scleractinia).

Deep-water coral reefs are found worldwide and harbor biodiversity levels that are comparable to their shallow-water counterparts. However, the genetic diversity and population structure of deep-water species remain poorly explored, and historical taxonomical issues still need to be resolved. Here we used microsatellite markers as well as ultraconserved elements (UCE) and exons to shed light on the population structure, genetic diversity, and phylogenetic position of the genus Madrepora, which contains M. oculata, one of the most widespread scleractinian species. Population structure of 107 samples from three Southwestern Atlantic sedimentary basins revealed the occurrence of a cryptic species, herein named M. piresae sp. nov. (authored by Kitahara, Capel and Zilberberg), which can be found in sympatry with M. oculata. Phylogeny reconstructions based on 134 UCEs and exon regions corroborated the population genetic data, with the recovery of two well-supported groups, and reinforced the polyphyly of the family Oculinidae. In order to better accommodate the genus Madrepora, while reducing taxonomical confusion associated with the name Madreporidae, we propose the monogeneric family Bathyporidae fam. nov. (authored by Kitahara, Capel, Zilberberg and Cairns). Our findings advance the knowledge on the widespread deep-water genus Madrepora, resolve a long-standing question regarding the phylogenetic position of the genus, and highlight the need of a worldwide review of the genus.

Marine Heatwave Caused Differentiated Dysbiosis in Photosymbiont Assemblages of Corals and Hydrocorals During El Niño 2015/2016.

Reef corals have been threatened by climate change, with more frequent and intense bleaching events leading to extensive coral mortality and loss of coral cover worldwide. In the face of this, the corals' photosymbiont assemblages have received special attention as a key to better understand the bleaching process and its recovery. To assess the effects of thermal anomalies, the coral Mussismilia harttii and the hydrocoral Millepora alcicornis were monitored through the El Niño 2015/2016 at a Southwestern Atlantic (SWA) coral reef. A severe bleaching event (57% of colonies bleached) was documented, triggered by a < 3 °C-week heatwave, but no mortality was detected. The hydrocoral was more susceptible than the scleractinian, displaying bleaching symptoms earlier and experiencing a longer and more intense bleaching event. The composition of photosymbionts in the M. alcicornis population was affected only at the rare biosphere level (< 5% relative abundance), with the emergence of new symbionts after bleaching. Conversely, a temporary dysbiosis was observed in the M. harttii population, with one of the dominant symbiodiniaceans decreasing in relative abundance at the peak of the bleaching, which negatively affected the total ß-diversity. After colonies' complete recovery, symbiodiniaceans' dominances returned to normal levels in both hosts. These results highlight critical differences in how the two coral species cope with bleaching and contribute to the understanding of the role of photosymbionts throughout the bleaching-recovery process.

Schools reopening and the COVID-19 pandemic: a case study from Macaé, Rio de Janeiro, Brazil.

Since the first reported case of COVID-19 in Brazil, the public and private educational system started to close. Up to November 2020, scientific discussions about the return of schooling activities have been rarely performed by the national scientific community and police-makers. The great delay of school returning in Brazil contrasts with successful international strategies of school reopening worldwide and seems counterintuitive with the reopening of non-essential activities. Here, important issues to be considered before and during school reopening are reviewed and discussed. COVID-19 testing is essential to avoid disease spreading, but high cost of individual RT-qPCRs impairs an extensive testing strategy for school returning. To reduce costs and increase the speed of diagnosis, we tested the efficiency of a pooled-sample PCR strategy in a cohort of the educational staff in the city of Macaé/RJ, finding five asymptomatic individuals (0,66%) among the 754 people tested. Thus, a polled-sample PCR testing strategy of the educational staff might prevent infection spreading in schools at a reasonable cost. We discuss how our test strategy could be coupled with internationally recognized safety rules to allow for a safe school return and how countries from different world regions are dealing with educational activities during COVID-19 pandemic.

Molecular testing and analysis of disease spreading during the emergence of COVID-19 in Macaé, the Brazilian National Capital of Oil.

The Brazilian strategy to overcome the spread of COVID-19 has been particularly criticized due to the lack of a national coordinating effort and an appropriate testing program. Here, a successful approach to control the spread of COVID-19 transmission is described by the engagement of public (university and governance) and private sectors (hospitals and oil companies) in Macaé, state of Rio de Janeiro, Brazil, a city known as the National Oil Capital. In 2020 between the 17th and 38th epidemiological week, over two percent of the 206,728 citizens were subjected to symptom analysis and RT-qPCR testing by the Federal University of Rio de Janeiro, with positive individuals being notified up to 48 h after swab collection. Geocodification and spatial cluster analysis were used to limit COVID-19 spreading in Macaé. Within the first semester after the outbreak of COVID-19 in Brazil, Macaé recorded 1.8% of fatalities associated with COVID-19 up to the 38th epidemiological week, which was at least five times lower than the state capital (10.6%). Overall, considering the successful experience of this joint effort of private and public engagement in Macaé, our data suggest that the development of a similar strategy countrywise could have contributed to a better control of the COVID-19 spread in Brazil. Quarantine decree by the local administration, comprehensive molecular testing coupled to scientific analysis of COVID-19 spreading, prevented the catastrophic consequences of the pandemic as seen in other populous cities within the state of Rio de Janeiro and elsewhere in Brazil.

Atlantia, a new genus of Dendrophylliidae (Cnidaria, Anthozoa, Scleractinia) from the eastern Atlantic.

Atlantia is described as a new genus pertaining to the family Dendrophylliidae (Anthozoa, Scleractinia) based on specimens from Cape Verde, eastern Atlantic. This taxon was first recognized as Enallopsammia micranthus and later described as a new species, Tubastraea caboverdiana, which then changed the status of the genus Tubastraea as native to the Atlantic Ocean. Here, based on morphological and molecular analyses, we compare fresh material of T. caboverdiana to other dendrophylliid genera and describe it as a new genus named Atlantia in order to better accommodate this species. Evolutionary reconstruction based on two mitochondrial and one nuclear marker for 67 dendrophylliids and one poritid species recovered A. caboverdiana as an isolated clade not related to Tubastraea and more closely related to Dendrophyllia cornigera and Leptopsammia pruvoti. Atlantia differs from Tubastraea by having a phaceloid to dendroid growth form with new corallites budding at an acute angle from the theca of a parent corallite. The genus also has normally arranged septa (not Portualès Plan), poorly developed columella, and a shallow-water distribution all supporting the classification as a new genus. Our results corroborate the monophyly of the genus Tubastraea and reiterate the Atlantic non-indigenous status for the genus. In the light of the results presented herein, we recommend an extensive review of shallow-water dendrophylliids from the Eastern Atlantic.

Correction: Biogeography of the endosymbiotic dinoflagellates (Symbiodiniaceae) community associated with the brooding coral Favia gravida in the Atlantic Ocean.

[This corrects the article DOI: 10.1371/journal.pone.0213519.].

Biogeography of the endosymbiotic dinoflagellates (Symbiodiniaceae) community associated with the brooding coral Favia gravida in the Atlantic Ocean.

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.

Clone wars: asexual reproduction dominates in the invasive range of Tubastraea spp. (Anthozoa: Scleractinia) in the South-Atlantic Ocean.

Although the invasive azooxanthellate corals Tubastraea coccinea and T. tagusensis are spreading quickly and outcompeting native species in the Atlantic Ocean, there is little information regarding the genetic structure and path of introduction for these species. Here we present the first data on genetic diversity and clonal structure from these two species using a new set of microsatellite markers. High proportions of clones were observed, indicating that asexual reproduction has a major role in the local population dynamics and, therefore, represents one of the main reasons for the invasion success. Although no significant population structure was found, results suggest the occurrence of multiple invasions for T. coccinea and also that both species are being transported along the coast by vectors such as oil platforms and monobouys, spreading these invasive species. In addition to the description of novel microsatellite markers, this study sheds new light into the invasive process of Tubastraea.

Broadcast Spawning Coral Mussismilia hispida Can Vertically Transfer its Associated Bacterial Core.

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.

Polymorphic Microsatellite Loci for Endemic Mussismilia Corals (Anthozoa: Scleractinia) of the Southwest Atlantic Ocean.

In the Southwest Atlantic, coral reefs are unique due to their growth form, low species richness, and a high level of endemic coral species, which include the most important reef builders. Although these reefs are the only true biogenic reefs in the South Atlantic Ocean, population genetic studies are still lacking. The purpose of this study was to develop a suite of microsatellite loci to help gain insights into the population diversity and connectivity of the endemic scleractinian coral with the largest distributional range along the Southwest Atlantic coast, Mussismilia hispida Fourteen microsatellite loci were characterized, and their degree of polymorphism was analyzed in 33 individuals. The number of alleles varied between 4 and 17 per loci, and H o varied between 0.156 and 0.928, with 2 loci showing significant heterozygote deficiency. Cross-amplification tests on the other 2 species of the genus (Mussismilia braziliensis and Mussismilia harttii) demonstrated that these markers are suitable for studies of population diversity and structure of all 3 species of Mussismilia Because they are the most important reef builders in the Southwest Atlantic, the developed microsatellite loci may be important tools for connectivity and conservation studies of these endemic corals.

Morphology and molecules on opposite sides of the diversity gradient: four cryptic species of the Cliona celata (Porifera, Demospongiae) complex in South America revealed by mitochondrial and nuclear markers.

A great number of marine organisms lack proper morphologic characters for identification and species description. This could promote a wide distributional pattern for a species morphotype, potentially generating many morphologically similar albeit evolutionarily independent worldwide lineages. This work aimed to estimate the genetic variation of South America populations of the Cliona celata species complex. We used COI mtDNA and ITS rDNA as molecular markers and tylostyle length and width as morphological characters to try to distinguish among species. Four distinct clades were found within the South American C. celata complex using both genetic markers. The genetic distances comparisons revealed that scores among those clades were comparable to distances between each clade and series of previously described clionaid species, some of which belong to different genera. Our results also suggest that one of the clades has a broad discontinuous distribution in the Atlantic Ocean, while another presents high gene flow between the southern Atlantic and Pacific coasts of South America. Conversely, spicule morphology was not able to distinguish each clade, due to the high degree of overlap among them. Therefore, we considered that each recovered clade correspond, in fact, to different species that cannot be differentiated via morphological characters, which are often used to describe species within the C. celata species complex.

Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment.

In the present study, we investigated the progressive acclimation of the mussel Mytilus galloprovincialis to different reduced seawater (SW) salinities and its effect on several biochemical markers and biotests. Mussels were purchased from a local mariculture facility during summer (SW temperature 27 degrees C, salinity 37.5 psu) and winter (13 degrees C, 37 psu) seasons, and transferred to the laboratory for acclimation to reduced SW salinities (37, 28, 18.5 and 11 psu). At the beginning and at the end of acclimation processes tests of mussel survival in air were provided. After 14 days of acclimation the DNA integrity, p38-MAPK activation, metallothionein induction, oxygen consumption rate, and condition index were measured. Survival in air (SOS test), as a physiological index of mussel's health and vitality, had significantly lower LT50 values (11 psu) in the summer than in the winter, and it seems to be negatively affected by acclimation in comparison to controls (37 psu and mariculture). Condition indexes (CIs) were not significantly different, but mussel's acclimation resulted in decline (i.e., a negative trend), especially of CI-2 and CI-3 calculated on the basis of mussel tissue weight and shell sizes. Oxygen consumption rate (VO2) of M. galloprovincialis acclimated to reduced salinities was a concentration-dependent process and increased considerably to about 51 and 65% in lower SW concentrations (28 and 18 psu) compared to control mussels (37 psu). DNA integrity, determined by Fast Micromethod, was negatively impacted by salinity acclimation and corresponding physiological stress as well. Some differences in 1D protein expression patterns between control groups and mussels acclimated to 28, 18.5 and 11 psu (SW) were established. Reduced SW salinities (18.5 and 11 psu) resulted in significantly higher p38-MAPK phosphorylation, whereas the SW salinity of 28 psu decreased p-p38 significantly compared to control (37 psu). The concentration of metallothioneins in mussels' gills was reduced at 28 and 18.5 psu, while it was significantly higher at 11 psu. Results indicated that SW salinity variation (i.e., hypoosmotic stress) in the marine environment can affect all investigated parameters. This investigation expands our understanding of multifactorial effects of the physical marine environment on the specificity of investigated biomarkers and biotests, providing insight into the acclimation, adaptive and stress response processes of mussels. Effects of environmental factors have to be considered in sampling strategies for monitoring programmes to prevent false interpretation of results.