Microbiomes of Thalassia testudinum throughout the Atlantic Ocean, Caribbean Sea, and Gulf of Mexico are influenced by site and region while maintaining a core microbiome.

Plant microbiomes are known to serve several important functions for their host, and it is therefore important to understand their composition as well as the factors that may influence these microbial communities. The microbiome of Thalassia testudinum has only recently been explored, and studies to-date have primarily focused on characterizing the microbiome of plants in a single region. Here, we present the first characterization of the composition of the microbial communities of T. testudinum across a wide geographical range spanning three distinct regions with varying physicochemical conditions. We collected samples of leaves, roots, sediment, and water from six sites throughout the Atlantic Ocean, Caribbean Sea, and the Gulf of Mexico. We then analyzed these samples using 16S rRNA amplicon sequencing. We found that site and region can influence the microbial communities of T. testudinum, while maintaining a plant-associated core microbiome. A comprehensive comparison of available microbial community data from T. testudinum studies determined a core microbiome composed of 14 ASVs that consisted mostly of the family Rhodobacteraceae. The most abundant genera in the microbial communities included organisms with possible plant-beneficial functions, like plant-growth promoting taxa, disease suppressing taxa, and nitrogen fixers.

Herbivore effects increase with latitude across the extent of a foundational seagrass.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment.

We present chromosome-level genome assemblies from representative species of three independently evolved seagrass lineages: Posidonia oceanica, Cymodocea nodosa, Thalassia testudinum and Zostera marina. We also include a draft genome of Potamogeton acutifolius, belonging to a freshwater sister lineage to Zosteraceae. All seagrass species share an ancient whole-genome triplication, while additional whole-genome duplications were uncovered for C. nodosa, Z. marina and P. acutifolius. Comparative analysis of selected gene families suggests that the transition from submerged-freshwater to submerged-marine environments mainly involved fine-tuning of multiple processes (such as osmoregulation, salinity, light capture, carbon acquisition and temperature) that all had to happen in parallel, probably explaining why adaptation to a marine lifestyle has been exceedingly rare. Major gene losses related to stomata, volatiles, defence and lignification are probably a consequence of the return to the sea rather than the cause of it. These new genomes will accelerate functional studies and solutions, as continuing losses of the 'savannahs of the sea' are of major concern in times of climate change and loss of biodiversity.

Seagrass structural and elemental indicators reveal high nutrient availability within a tropical lagoon in Panama.

Seagrass meadows are valued coastal habitats that provide ecological and economic benefits around the world. Despite their importance, many meadows are in decline, driven by a variety of anthropogenic impacts. While these declines have been well documented in some regions, other locations (particularly within the tropics) lack long-term monitoring programs needed to resolve seagrass trends over time. Effective and spatially-expansive monitoring within under-represented regions is critical to provide an accurate perspective on seagrass status and trends. We present a comprehensive dataset on seagrass coverage and composition across 24 sites in Bahía Almirante, a lagoon along the Caribbean coast of Panama. Using a single survey, we focus on capturing spatial variation in seagrass physical and elemental characteristics and provide data on key seagrass bio-indicators, such as leaf morphology (length and width), elemental content (% nitrogen and phosphorus) and stable isotopic signatures (δ 13C and δ 15N). We further explore relationships between these variables and water depth (proxy for light availability) and proximity to shore (proxy for terrestrial inputs). The seagrass assemblage was mostly monospecific (dominated by Thalassia testudinum) and restricted to shallow water (<3 m). Above-ground biomass varied widely, averaging 71.7 g dry mass m-2, yet ranging from 24.8 to 139.6 g dry mass m-2. Leaf nitrogen content averaged 2.2%, ranging from 1.76 to 2.57%, while phosphorus content averaged 0.19% and ranged from 0.15 to 0.23%. These values were high compared to other published reports for T. testudinum, indicating elevated nutrient availability within the lagoon. Seagrass stable isotopic characteristics varied slightly and were comparable with other published values. Leaf carbon signatures (δ 13C) ranged from -11.74 to -6.70‰ and were positively correlated to shoreline proximity, suggesting a contribution of terrestrial carbon to seagrass biomass. Leaf nitrogen signatures (δ 15N) ranged from -1.75 to 3.15‰ and showed no correlation with shoreline proximity, suggesting that N sources within the bay were not dominated by localized point-source discharge of treated sewage. Correlations between other seagrass bio-indicators and environmental metrics were mixed: seagrass cover declined with depth, while biomass was negatively correlated with N, indicating that light and nutrient availability may jointly regulate seagrass cover and biomass. Our work documents the response of seagrass in Bahía Almirante to light and nutrient availability and highlights the eutrophic status of this bay. Using the broad spatial coverage of our survey as a baseline, we suggest the future implementation of a continuous and spatially expansive seagrass monitoring program within this region to assess the health of these important systems subject to global and local stressors.

Effects of future climate on coral-coral competition.

As carbon dioxide (CO2) levels increase, coral reefs and other marine systems will be affected by the joint stressors of ocean acidification (OA) and warming. The effects of these two stressors on coral physiology are relatively well studied, but their impact on biotic interactions between corals are poorly understood. While coral-coral interactions are less common on modern reefs, it is important to document the nature of these interactions to better inform restoration strategies in the face of climate change. Using a mesocosm study, we evaluated whether the combined effects of ocean acidification and warming alter the competitive interactions between the common coral Porites astreoides and two other mounding corals (Montastraea cavernosa or Orbicella faveolata) common in the Caribbean. After 7 days of direct contact, P. astreoides suppressed the photosynthetic potential of M. cavernosa by 100% in areas of contact under both present (~28.5°C and ~400 µatm pCO2) and predicted future (~30.0°C and ~1000 µatm pCO2) conditions. In contrast, under present conditions M. cavernosa reduced the photosynthetic potential of P. astreoides by only 38% in areas of contact, while under future conditions reduction was 100%. A similar pattern occurred between P. astreoides and O. faveolata at day 7 post contact, but by day 14, each coral had reduced the photosynthetic potential of the other by 100% at the point of contact, and O. faveolata was generating larger lesions on P. astreoides than the reverse. In the absence of competition, OA and warming did not affect the photosynthetic potential of any coral. These results suggest that OA and warming can alter the severity of initial coral-coral interactions, with potential cascading effects due to corals serving as foundation species on coral reefs.

Re-modeling of foliar membrane lipids in a seagrass allows for growth in phosphorus-deplete conditions.

In this study, we used liquid chromatography high-resolution tandem mass spectrometry to analyze the lipidome of turtlegrass (Thalassia testudinum) leaves with either extremely high phosphorus content or extremely low phosphorus content. Most species of phospholipids were significantly down-regulated in phosphorus-deplete leaves, whereas diacylglyceryltrimethylhomoserine (DGTS), triglycerides (TG), galactolipid digalactosyldiacylglycerol (DGDG), certain species of glucuronosyldiacylglycerols (GlcADG), and certain species of sulfoquinovosyl diacylglycerol (SQDG) were significantly upregulated, accounting for the change in phosphorus content, as well as structural differences in the leaves of plants growing across regions of varying elemental availability. These data suggest that seagrasses are able to modify the phosphorus content in leaf membranes dependent upon environmental availability.

Chemical and Metagenomic Studies of the Lethal Black Band Disease of Corals Reveal Two Broadly Distributed, Redox-Sensitive Mixed Polyketide/Peptide Macrocycles.

Black band disease (BBD), a lethal, polymicrobial disease consortium dominated by the cyanobacterium Roseofilum reptotaenium, kills many species of corals worldwide. To uncover chemical signals or cytotoxins that could be important in proliferation of Roseofilum and the BBD layer, we examined the secondary metabolites present in geographically diverse collections of BBD from Caribbean and Pacific coral reefs. Looekeyolide A (1), a 20-membered macrocyclic compound formed by a 16-carbon polyketide chain, 2-deamino-2-hydroxymethionine, and d-leucine, and its autoxidation product looekeyolide B (2) were extracted as major compounds (∼1 mg g-1 dry wt) from more than a dozen field-collected BBD samples. Looekeyolides A and B were also produced by a nonaxenic R. reptotaenium culture under laboratory conditions at similar concentrations. R. reptotaenium genomes that were constructed from four different metagenomic data sets contained a unique nonribosomal peptide/polyketide biosynthetic cluster that is likely responsible for the biosynthesis of the looekeyolides. Looekeyolide A, which readily oxidizes to looekeyolide B, may play a biological role in reducing H2O2 and other reactive oxygen species that could occur in the BBD layer as it overgrows and destroys coral tissue.

Squidpops: A Simple Tool to Crowdsource a Global Map of Marine Predation Intensity.

We present a simple, standardized assay, the squidpop, for measuring the relative feeding intensity of generalist predators in aquatic systems. The assay consists of a 1.3-cm diameter disk of dried squid mantle tethered to a rod, which is either inserted in the sediment in soft-bottom habitats or secured to existing structure. Each replicate squidpop is scored as present or absent after 1 and 24 hours, and the data for analysis are proportions of replicate units consumed at each time. Tests in several habitats of the temperate southeastern USA (Virginia and North Carolina) and tropical Central America (Belize) confirmed the assay's utility for measuring variation in predation intensity among habitats, among seasons, and along environmental gradients. In Belize, predation intensity varied strongly among habitats, with reef > seagrass = mangrove > unvegetated bare sand. Quantitative visual surveys confirmed that assayed feeding intensity increased with abundance and species richness of fishes across sites, with fish abundance and richness explaining up to 45% and 70% of the variation in bait loss respectively. In the southeastern USA, predation intensity varied seasonally, being highest during summer and declining in late autumn. Deployments in marsh habitats generally revealed a decline in mean predation intensity from fully marine to tidal freshwater sites. The simplicity, economy, and standardization of the squidpop assay should facilitate engagement of scientists and citizens alike, with the goal of constructing high-resolution maps of how top-down control varies through space and time in aquatic ecosystems, and addressing a broad array of long-standing hypotheses in macro- and community ecology.