Dominance of the coral Pocillopora acuta around Phuket Island in the Andaman Sea, Thailand.

Pocillopora damicornis (Linnaeus, 1758), a species complex, consists of several genetic lineages, some of which likely represent reproductively isolated species, including the species Pocillopora acuta Lamarck, 1816. Pocillopora acuta can exhibit similar morphological characteristics as P. damicornis, thus making it difficult to identify species-level taxonomic units. To determine whether the P. damicornis-like colonies on the reefs in the Andaman Sea (previously often identified as P. damicornis) consist of different species, we sampled individual colonies at five sites along a 50 km coastal stretch at Phuket Island and four island sites towards Krabi Province, Thailand. We sequenced 210 coral samples for the mitochondrial open reading frame and identified six distinct haplotypes, all belonging to P. acuta according to the literature. Recently, P. acuta was observed to efficiently recolonize heat-damaged reefs in Thailand as well as globally, making it a potentially important coral species in future reefs. Specifically in the light of global change, this study underscores the importance of high-resolution molecular species recognition, since taxonomic units are important factors for population genetic studies, and the latter are crucial for management and conservation efforts.

Population genetic differentiation of the ubiquitous brooding coral Pocillopora acuta along Phuket Island reefs in the Andaman Sea, Thailand.

BACKGROUND: The widespread Indo-Pacific coral species Pocillopora acuta Lamarck, 1816 displays varying levels of asexual versus sexual reproduction, with strong repercussions on genetic diversity, connectivity and genetic structuring within and among populations. For many geographic regions, baseline information on genetic diversity is still lacking, particularly in the Andaman Sea. The region suffered a massive heat-induced bleaching event in 2010 with high coral cover loss of branching coral species such as P. acuta. A subsequent bleaching in 2016, however, revealed a mild bleaching response in pocilloporids compared to other coral taxa in the region, suggesting that rare, heat tolerant genotypes had been selected by the 2010 bleaching event. In order to test whether this potential 'evolutionary rescue' event has led to a low genetic diversity, we conducted a population genetic survey covering a total of nine different P. acuta populations (336 individuals) along a 50 km coastal stretch around Phuket Island, Thailand. We used six microsatellite markers to assess genotypic diversity and to determine the prevalent mode of reproduction (i.e. sexual or asexual recruitment). RESULTS: In contrast to other Indian Ocean P. acuta populations, the majority of corals in this study adopted a sexual reproduction mode (75% across all populations). At the same time, substantial regional gene flow was observed around Phuket Island with strong genetic differentiation as indicated by three genetic clusters that were separated by only a few kilometers. Patterns of isolation by distance over 0.7 - 40 km suggest small-scale genetic barriers, such as changing currents throughout each monsoonal season, potentially contributing to locally restricted dispersal of P. acuta larvae. CONCLUSIONS: The occurrence of distinct genetic clusters within short coastal stretches suggests that the 2010 bleaching event has not led to extreme genetic impoverishment. While more in-depth genomic analyses are necessary to investigate changes in genetic diversity following extreme bleaching events, our results will help guide conservation efforts to maintain genetic diversity of a coral species that likely will be dominant in future, warmer Andaman Sea reefs.

Towards enhancing coral heat tolerance: a "microbiome transplantation" treatment using inoculations of homogenized coral tissues.

BACKGROUND: Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. RESULTS: Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context. CONCLUSIONS: Our results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect. Video abstract.

The Indian Ocean Dipole and El Niño Southern Oscillation as major drivers of coral cover on shallow reefs in the Andaman Sea.

Shallow reefs are a major feature of coral assemblages in the Andaman Sea. At Phuket, Thailand sheltered reefs are dominated by massive corals, together with an increasing abundance of branching species during favourable growth conditions. The growth of coral on these reefs is moderated by long-term increases in sea temperature and relative sea level but fluctuating decadal/intradecadal climate processes of El Niño Southern Oscillation (ENSO) and Indian Ocean Dipole (IOD), which modulate sea level and temperature, are the main drivers of coral cover. In this study, the contribution of these two climate processes was identified and also quantified. Over a 34-year study of fluctuating coral cover, the three major reductions in cover in 1997, 2010 and 2019 were linked to overlapping positive IOD (pIOD) and El Niños in 1997 and 2019, and with an El Niño alone in 2010. Combined pIOD and El Niño depressed sea level was the major factor in reducing cover in 1997 while El Niño extreme sea temperatures were responsible for large reductions in 2010. In 2019, a bi-phasic pIOD and El Niño resulted in lowered cover at a time of both decreased sea level and high sea temperature. Under global warming scenarios, it is projected that extreme pIODs, such as those seen in 1997 and 2019, will occur more frequently while El Niño frequencies will continue to increase even after global mean temperature stabilization. In these circumstances, and with steadily rising background sea temperatures, the future risks to the shallow reefs of the Andaman Sea are substantial, despite any temporary respite gained from climate related or land subsidence sea-level rise. Such findings have wider implications for all reefs affected by climatic-driven sea-level depressions, particularly those around Indonesian shores where similar El-Niño-related reductions in coral cover have been reported.

Heat-induced shift in coral microbiome reveals several members of the Rhodobacteraceae family as indicator species for thermal stress in Porites lutea.

The coral holobiont is a complex ecosystem consisting of coral animals and a highly diverse consortium of associated microorganisms including algae, fungi, and bacteria. Several studies have highlighted the importance of coral-associated bacteria and their potential roles in promoting the host fitness and survival. Recently, dynamics of coral-associated microbiomes have been demonstrated to be linked to patterns of coral heat tolerance. Here, we examined the effect of elevated seawater temperature on the structure and diversity of bacterial populations associated with Porites lutea, using full-length 16S rRNA sequences obtained from Pacific Biosciences circular consensus sequencing. We observed a significant increase in alpha diversity indices and a distinct shift in microbiome composition during thermal stress. There was a marked decline in the apparent relative abundance of Gammaproteobacteria family Endozoicomonadaceae after P. lutea had been exposed to elevated seawater temperature. Concomitantly, the bacterial community structure shifted toward the predominance of Alphaproteobacteria family Rhodobacteraceae. Interestingly, we did not observe an increase in relative abundance of Vibrio-related sequences in our heat-stressed samples even though the appearance of Vibrio spp. has often been detected in parallel with the increase in the relative abundance of Rhodobacteraceae during thermal bleaching in other coral species. The ability of full-length 16S rRNA sequences in resolving taxonomic uncertainty of associated bacteria at a species level enabled us to identify 24 robust indicator bacterial species for thermally stressed corals. It is worth noting that the majority of those indicator species were members of the family Rhodobacteraceae. The comparison of bacterial community structure and diversity between corals in ambient water temperature and thermally stressed corals may provide a better understanding on how bacteria symbionts contribute to the resilience of their coral hosts to ocean warming.

Dynamics of coral-associated microbiomes during a thermal bleaching event.

Coral-associated microorganisms play an important role in their host fitness and survival. A number of studies have demonstrated connections between thermal tolerance in corals and the type/relative abundance of Symbiodinium they harbor. More recently, the shifts in coral-associated bacterial profiles were also shown to be linked to the patterns of coral heat tolerance. Here, we investigated the dynamics of Porites lutea-associated bacterial and algal communities throughout a natural bleaching event, using full-length 16S rRNA and internal transcribed spacer sequences (ITS) obtained from PacBio circular consensus sequencing. We provided evidence of significant changes in the structure and diversity of coral-associated microbiomes during thermal stress. The balance of the symbiosis shifted from a predominant association between corals and Gammaproteobacteria to a predominance of Alphaproteobacteria and to a lesser extent Betaproteobacteria following the bleaching event. On the contrary, the composition and diversity of Symbiodinium communities remained unaltered throughout the bleaching event. It appears that the switching and/or shuffling of Symbiodinium types may not be the primary mechanism used by P. lutea to cope with increasing seawater temperature. The shifts in the structure and diversity of associated bacterial communities may contribute more to the survival of the coral holobiont under heat stress.

High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system.

Coral reefs are a complex ecosystem consisting of coral animals and a vast array of associated symbionts including the dinoflagellate Symbiodinium, fungi, viruses and bacteria. Several studies have highlighted the importance of coral-associated bacteria and their fundamental roles in fitness and survival of the host animal. The scleractinian coral Porites lutea is one of the dominant reef-builders in the Indo-West Pacific. Currently, very little is known about the composition and structure of bacterial communities across P. lutea reefs. The purpose of this study is twofold: to demonstrate the advantages of using PacBio circular consensus sequencing technology in microbial community studies and to investigate the diversity and structure of P. lutea-associated microbiome in the Indo-Pacific. This is the first metagenomic study of marine environmental samples that utilises the PacBio sequencing system to capture full-length 16S rRNA sequences. We observed geographically distinct coral-associated microbial profiles between samples from the Gulf of Thailand and Andaman Sea. Despite the geographical and environmental impacts on the coral-host interactions, we identified a conserved community of bacteria that were present consistently across diverse reef habitats. Finally, we demonstrated the superior performance of full-length 16S rRNA sequences in resolving taxonomic uncertainty of coral associates at the species level.

Age-Related Shifts in Bacterial Diversity in a Reef Coral.

This study investigated the relationship between microbial communities in differently sized colonies of the massive coral Coelastrea aspera at Phuket, Thailand where colony size could be used as a proxy for age. Results indicated significant differences between the bacterial diversity (ANOSIM, R = 0.76, p = 0.001) of differently sized colonies from the same intertidal reef habitat. Juvenile and small colonies (< 6 cm mean diam) harboured a lower bacterial richness than medium (~ 10 cm mean diam) and large colonies (> 28 cm mean diam). Bacterial diversity increased in a step-wise pattern from juveniles < small < medium colonies, which was then followed by a slight decrease in the two largest size classes. These changes appear to resemble a successional process which occurs over time, similar to that observed in the ageing human gut. Furthermore, the dominant bacterial ribotypes present in the tissues of medium and large sized colonies of C. aspera, (such as Halomicronema, an Oscillospira and an unidentified cyanobacterium) were also the dominant ribotypes found within the endolithic algal band of the coral skeleton; a result providing some support for the hypothesis that the endolithic algae of corals may directly influence the bacterial community present in coral tissues.