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1. A Phylogeny-Informed Analysis of the Global Coral-Symbiodiniaceae Interaction Network Reveals that Traits Correlated with Thermal Bleaching Are Specific to Symbiont Transmission Mode

   https://doi.org/10.1128/mSystems.00266-21  

   Swain, Timothy D.; Lax, Simon; Gilbert, Jack; Backman, Vadim; Marcelino, Luisa A. (June 2021, mSystems)

   Bik, Holly (Ed.)

   ABSTRACT The complex network of associations between corals and their dinoflagellates (family Symbiodiniaceae) are the basis of coral reef ecosystems but are sensitive to increasing global temperatures. Coral-symbiont interactions are restricted by ecological and evolutionary determinants that constrain partner choice and influence holobiont response to environmental stress; however, little is known about how these processes shape thermal resilience of the holobiont. Here, we built a network of global coral-Symbiodiniaceae associations, mapped species traits (e.g., symbiont transmission mode and biogeography) and phylogenetic relationships of both partners onto the network, and assigned thermotolerance to both host and symbiont nodes. Using network analysis and phylogenetic comparative methods, we determined the contribution of species traits to thermal resilience of the holobiont, while accounting for evolutionary patterns among species. We found that the network shows nonrandom interactions among species, which are shaped by evolutionary history, symbiont transmission mode (horizontally transmitted [HT] or vertically transmitted [VT] corals) and biogeography. Coral phylogeny, but not Symbiodiniaceae phylogeny, symbiont transmission mode, or biogeography, was a good predictor of thermal resilience. Closely related corals have similar Symbiodiniaceae interaction patterns and bleaching susceptibilities. Nevertheless, the association patterns that explain increased host thermal resilience are not generalizable across the entire network but are instead unique to HT and VT corals. Under nonstress conditions, thermally resilient VT coral species associate with thermotolerant phylotypes and limit their number of unique symbionts and overall symbiont thermotolerance diversity, while thermally resilient HT coral species associate with a few host-specific symbiont phylotypes. IMPORTANCE Recent advances have revealed a complex network of interactions between coral and Symbiodiniaceae. Specifically, nonrandom association patterns, which are determined in part by restrictions imposed by symbiont transmission mode, increase the sensitivity of the overall network to thermal stress. However, little is known about the extent to which coral-Symbiodiniaceae network resistance to thermal stress is shaped by host and symbiont species phylogenetic relationships and host and symbiont species traits, such as symbiont transmission mode. We built a frequency-weighted global coral-Symbiodiniaceae network and used network analysis and phylogenetic comparative methods to show that evolutionary relatedness, but not transmission mode, predicts thermal resilience of the coral-Symbiodiniaceae holobiont. Consequently, thermal stress events could result in nonrandom pruning of susceptible lineages and loss of taxonomic diversity with catastrophic effects on community resilience to future events. Our results show that inclusion of the contribution of evolutionary and ecological processes will further our understanding of the fate of coral assemblages under climate change. 

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2. A holobiont view of island biogeography: Unravelling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates

   https://doi.org/10.1111/mec.16301  

   Armstrong, Ellie E.; Perez‐Lamarque, Benoît; Bi, Ke; Chen, Cerise; Becking, Leontine E.; Lim, Jun Ying; Linderoth, Tyler; Krehenwinkel, Henrik; Gillespie, Rosemary G. (December 2021, Molecular Ecology)

   Abstract The diversification of a host lineage can be influenced by both the external environment and its assemblage of microbes. Here, we use a young lineage of spiders, distributed along a chronologically arranged series of volcanic mountains, to investigate how their associated microbial communities have changed as the spiders colonized new locations. Using the stick spiderAriamnes waikula(Araneae, Theridiidae) on the island of Hawaiʻi, and outgroup taxa on older islands, we tested whether each component of the “holobiont” (spider hosts, intracellular endosymbionts and gut microbial communities) showed correlated signatures of diversity due to sequential colonization from older to younger volcanoes. To investigate this, we generated ddRAD data for the host spiders and 16S rRNA gene amplicon data from their microbiota. We expected sequential colonizations to result in a (phylo)genetic structuring of the host spiders and in a diversity gradient in microbial communities. The results showed that the hostA.waikulais indeed structured by geographical isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different betweenAriamnesspecies on different islands, but more homogeneous amongA.waikulapopulations on the island of Hawaiʻi. Conversely, the gut microbiota, which we suspect is generally environmentally derived, was largely conserved across all populations and species. Our results show that different components of the holobiont respond in distinct ways to the dynamic environment of the volcanic archipelago. This highlights the necessity of understanding the interplay between different components of the holobiont, to properly characterize its evolution. 

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3. Eukaryotic algal community composition in tropical environments from solar salterns to the open sea

   https://doi.org/10.3389/fmars.2023.1131351  

   Eckmann, Charlotte A.; Eberle, Jessica S.; Wittmers, Fabian; Wilken, Susanne; Bergauer, Kristin; Poirier, Camille; Blum, Marguerite; Makareviciute-Fichtner, Kriste; Jimenez, Valeria; Bachy, Charles; et al (June 2023, Frontiers in Marine Science)

   Tropical environments with unique abiotic and biotic factors—such as salt ponds, mangroves, and coral reefs—are often in close proximity. The heterogeneity of these environments is reflected in community shifts over short distances, resulting in high biodiversity. While phytoplankton assemblages physically associated with corals, particularly their symbionts, are well studied, less is known about phytoplankton diversity across tropical aquatic environments. We assess shifts in phytoplankton community composition along inshore to offshore gradients by sequencing and analyzing 16S rRNA gene amplicons using primers targeting the V1-V2 region that capture plastids from eukaryotic phytoplankton and cyanobacteria, as well as heterotrophic bacteria. Microbial alpha diversity computed from 16S V1-V2 amplicon sequence variant (ASV) data from 282 samples collected in and around Curaçao, in the Southern Caribbean Sea, varied more within the dynamic salt ponds, salterns, and mangroves, compared to the seemingly stable above-reef, off-reef, and open sea environments. Among eukaryotic phytoplankton, stramenopiles often exhibited the highest relative abundances in mangrove, above-reef, off-reef, and open sea environments, where cyanobacteria also showed high relative abundances. Within stramenopiles, diatom amplicons dominated in salt ponds and mangroves, while dictyochophytes and pelagophytes prevailed above reefs and offshore. Green algae and cryptophytes were also present, and the former exhibited transitions following the gradient from inland to offshore. Chlorophytes and prasinophyte Class IV dominated in salt ponds, while prasinophyte Class II, including Micromonas commoda and Ostreococcus Clade OII, had the highest relative abundances of green algae in mangroves, above-reef, off-reef, and the open sea. To improve Class II prasinophyte classification, we sequenced 18S rRNA gene amplicons from the V4 region in 41 samples which were used to interrelate plastid-based results with information on uncultured prasinophyte species from prior 18S rRNA gene-based studies. This highlighted the presence of newly described Ostreococcus bengalensis and two Micromonas candidate species. Network analyses identified co-occurrence patterns between individual phytoplankton groups, including cyanobacteria, and heterotrophic bacteria. Our study reveals multiple uncultured and novel lineages within green algae and dictyochophytes in tropical marine habitats. Collectively, the algal diversity patterns and potential co-occurrence relationships observed in connection to physicochemical and spatial influences help provide a baseline against which future change can be assessed. 

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4. Antibiotics reduce Pocillopora coral‐associated bacteria diversity, decrease holobiont oxygen consumption and activate immune gene expression

   https://doi.org/10.1111/mec.17049  

   Connelly, Michael T.; Snyder, Grace; Palacio‐Castro, Ana M.; Gillette, Phillip R.; Baker, Andrew C.; Traylor‐Knowles, Nikki (August 2023, Molecular Ecology)

   Abstract Corals are important models for understanding invertebrate host–microbe interactions; however, to fully discern mechanisms involved in these relationships, experimental approaches for manipulating coral–bacteria associations are needed. Coral‐associated bacteria affect holobiont health via nutrient cycling, metabolic exchanges and pathogen exclusion, yet it is not fully understood how bacterial community shifts affect holobiont health and physiology. In this study, a combination of antibiotics (ampicillin, streptomycin and ciprofloxacin) was used to disrupt the bacterial communities of 14 colonies of the reef framework‐building corals Pocillopora meandrina and P .  verrucosa, originally collected from Panama and hosting diverse algal symbionts (family Symbiodiniaceae ). Symbiodiniaceae photochemical efficiencies and holobiont oxygen consumption (as proxies for coral health) were measured throughout a 5‐day exposure. Antibiotics altered bacterial community composition and reduced alpha and beta diversity, however, several bacteria persisted, leading to the hypothesis that these bacteria are either antibiotics resistant or occupy internal niches that are shielded from antibiotics. While antibiotics did not affect Symbiodiniaceae photochemical efficiency, antibiotics‐treated corals had lower oxygen consumption rates. RNAseq revealed that antibiotics increased expression of Pocillopora immunity and stress response genes at the expense of cellular maintenance and metabolism functions. Together, these results reveal that antibiotic disruption of corals' native bacteria negatively impacts holobiont health by decreasing oxygen consumption and activating host immunity without directly impairing Symbiodiniaceae photosynthesis, underscoring the critical role of coral‐associated bacteria in holobiont health. They also provide a baseline for future experiments that manipulate Pocillopora corals' symbioses by first reducing the diversity and complexity of coral‐associated bacteria. 

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5. Cassiopea xamachana microbiome across anatomy, development, and geography

   https://doi.org/10.1371/journal.pone.0319944  

   Kerwin, Allison H; Ohdera, Aki; Bier, Juliet; Goodman, Devon; Mammone, Marta; Sharp, Victoria; Echeandía, Alesandra; Medina, Mónica (April 2025, PLOS ONE)

   Sucharitakul, Phuping (Ed.)

   The upside-down jellyfish holobiont,Cassiopea xamachana, is a useful model system for tri-partite interactions between the cnidarian host, the photosymbiont, and the bacterial microbiome. While the interaction between the host and photosymbiont has been well studied, less is understood of the associated bacterial community. To date, the bacterial microbiome of wildC. xamachanahas remained largely uncharacterized. Thus, wild medusae (n=6) and larvae (n=3) were collected from two sites in the Florida Keys. Bacterial community composition was characterized via amplicon sequencing of the 16S rRNA gene V4 region. The medusa bacterial community was dominated by members of the Alphaproteobacteria and Gammaproteobacteria, while Planctomycetota, Actinomycetota, Bacteroidota, and Bacillota were also present, among others. Community composition was consistent between locations and across medusa structures (oral arm, bell, and gonad). The larval bacterial community clustered apart from the medusa community in beta diversity analysis and was characterized by the presence of several Pseudomonadota taxa that were not present in the medusa, including theAlteromonas,Pseudoalteromonas, andThalassobiusgenera. A bacterial isolate library encompassing much of the amplicon sequencing diversity was also developed and tested via metabolic assays in a separate culture-dependent analysis of isolates from medusa bells, oral arms, and laplets. Most characteristics were not correlated with host sex or medusa structure, but gelatinase production was more common in laplet isolates, while lactose fermentation was more common in female oral arm isolates. TheEndozoicomonasgenus was dominant in both amplicon sequencing and in our isolate library, and was equally prevalent across all medusa structures and in both sexes. Understanding the bacterial component of theC. xamachanaholobiont will allow us to further develop this important model cnidarian holobiont. 

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