Oceanographic drivers of deep-sea coral species distribution and community assembly on seamounts, islands, atolls, and reefs within the Phoenix Islands Protected Area

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Auscavitch, S. R., Deere, M. C., Keller, A. G., Rotjan, R. D., Shank, T. M., & Cordes, E. E. Oceanographic drivers of deep-sea coral species distribution and community assembly on seamounts, islands, atolls, and reefs within the Phoenix Islands Protected Area. Frontiers in Marine Science, 7, (2020): 42, doi:10.3389/fmars.2020.00042.The Phoenix Islands Protected Area, in the central Pacific waters of the Republic of Kiribati, is a model for large marine protected area (MPA) development and maintenance, but baseline records of the protected biodiversity in its largest environment, the deep sea (>200 m), have not yet been determined. In general, the equatorial central Pacific lacks biogeographic perspective on deep-sea benthic communities compared to more well-studied regions of the North and South Pacific Ocean. In 2017, explorations by the NOAA ship Okeanos Explorer and R/V Falkor were among the first to document the diversity and distribution of deep-water benthic megafauna on numerous seamounts, islands, shallow coral reef banks, and atolls in the region. Here, we present baseline deep-sea coral species distribution and community assembly patterns within the Scleractinia, Octocorallia, Antipatharia, and Zoantharia with respect to different seafloor features and abiotic environmental variables across bathyal depths (200–2500 m). Remotely operated vehicle (ROV) transects were performed on 17 features throughout the Phoenix Islands and Tokelau Ridge Seamounts resulting in the observation of 12,828 deep-water corals and 167 identifiable morphospecies. Anthozoan assemblages were largely octocoral-dominated consisting of 78% of all observations with seamounts having a greater number of observed morphospecies compared to other feature types. Overlying water masses were observed to have significant effects on community assembly across bathyal depths. Revised species inventories further suggest that the protected area it is an area of biogeographic overlap for Pacific deep-water corals, containing species observed across bathyal provinces in the North Pacific, Southwest Pacific, and Western Pacific. These results underscore significant geographic and environmental complexity associated with deep-sea coral communities that remain in under-characterized in the equatorial central Pacific, but also highlight the additional efforts that need to be brought forth to effectively establish baseline ecological metrics in data deficient bathyal provinces.Funding for this work was provided by NOAA Office of Ocean Exploration and Research (Grant No. NA17OAR0110083) to RR, EC, TS, and David Gruber

Modeling the Mutualistic Interactions between Tubeworms and Microbial Consortia

The deep-sea vestimentiferan tubeworm Lamellibrachia luymesi forms large aggregations at hydrocarbon seeps in the Gulf of Mexico that may persist for over 250 y. Here, we present the results of a diagenetic model in which tubeworm aggregation persistence is achieved through augmentation of the supply of sulfate to hydrocarbon seep sediments. In the model, L. luymesi releases the sulfate generated by its internal, chemoautotrophic, sulfide-oxidizing symbionts through posterior root-like extensions of its body. The sulfate fuels sulfate reduction, commonly coupled to anaerobic methane oxidation and hydrocarbon degradation by bacterial–archaeal consortia. If sulfate is released by the tubeworms, sulfide generation mainly by hydrocarbon degradation is sufficient to support moderate-sized aggregations of L. luymesi for hundreds of years. The results of this model expand our concept of the potential benefits derived from complex interspecific relationships, in this case involving members of all three domains of life

Growth and feeding of deep-sea coral Lophelia pertusa from the California margin under simulated ocean acidification conditions

The global decrease in seawater pH known as ocean acidification has important ecological consequences and is an imminent threat for numerous marine organisms. Even though the deep sea is generally considered to be a stable environment, it can be dynamic and vulnerable to anthropogenic disturbances including increasing temperature, deoxygenation, ocean acidification and pollution. Lophelia pertusa is among the better-studied cold-water corals but was only recently documented along the US West Coast, growing in acidified conditions. In the present study, coral fragments were collected at ∼300 m depth along the southern California margin and kept in recirculating tanks simulating conditions normally found in the natural environment for this species. At the collection site, waters exhibited persistently low pH and aragonite saturation states (Ωarag) with average values for pH of 7.66 ± 0.01 and Ωarag of 0.81 ± 0.07. In the laboratory, fragments were grown for three weeks in “favorable” pH/Ωarag of 7.9/1.47 (aragonite saturated) and “unfavorable” pH/Ωarag of 7.6/0.84 (aragonite undersaturated) conditions. There was a highly significant treatment effect (P < 0.001) with an average% net calcification for favorable conditions of 0.023 ± 0.009% d−1 and net dissolution of −0.010 ± 0.014% d-1 for unfavorable conditions. We did not find any treatment effect on feeding rates, which suggests that corals did not depress feeding in low pH/ Ωarag in an attempt to conserve energy. However, these results suggest that the suboptimal conditions for L. pertusa from the California margin could potentially threaten the persistence of this cold-water coral with negative consequences for the future stability of this already fragile ecosystem

Capacity of deep‐sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization

Cold seeps in the deep sea harbor various animals that have adapted to utilize seepage chemicals with the aid of chemosynthetic microbes that serve as primary producers. Corals are among the animals that live near seep habitats and yet, there is a lack of evidence that corals gain benefits and/or incur costs from cold seeps. Here, we focused on Callogorgia delta and Paramuricea sp. type B3 that live near and far from visual signs of currently active seepage at five sites in the deep Gulf of Mexico. We tested whether these corals rely on chemosynthetically-derived food in seep habitats and how the proximity to cold seeps may influence; (i) coral colony traits (i.e., health status, growth rate, regrowth after sampling, and branch loss) and associated epifauna, (ii) associated microbiome, and (iii) host transcriptomes. Stable isotope data showed that many coral colonies utilized chemosynthetically derived food, but the feeding strategy differed by coral species. The microbiome composition of C. delta, unlike Paramuricea sp., varied significantly between seep and non-seep colonies and both coral species were associated with various sulfur-oxidizing bacteria (SUP05). Interestingly, the relative abundances of SUP05 varied among seep and non-seep colonies and were strongly correlated with carbon and nitrogen stable isotope values. In contrast, the proximity to cold seeps did not have a measurable effect on gene expression, colony traits, or associated epifauna in coral species. Our work provides the first evidence that some corals may gain benefits from living near cold seeps with apparently limited costs to the colonies. Cold seeps provide not only hard substrate but also food to cold-water corals. Furthermore, restructuring of the microbiome communities (particularly SUP05) is likely the key adaptive process to aid corals in utilizing seepage-derived carbon. This highlights that those deep-sea corals may upregulate particular microbial symbiont communities to cope with environmental gradients

Structural and Functional MRI Differences in Master Sommeliers: A Pilot Study on Expertise in the Brain

Our experiences, even as adults, shape our brains. Regional differences have been found in experts, with the regions associated with their particular skill-set. Functional differences have also been noted in brain activation patterns in some experts. This study uses multimodal techniques to assess structural and functional patterns that differ between experts and nonexperts. Sommeliers are experts in wine and thus in olfaction. We assessed differences in Master Sommeliers’ brains, compared with controls, in structure and also in functional response to olfactory and visual judgment tasks. MRI data were analyzed using voxel-based morphometry as well as automated parcellation to assess structural properties, and group differences between tasks were calculated. Results indicate enhanced volume in the right insula and entorhinal cortex, with the cortical thickness of the entorhinal correlating with experience. There were regional activation differences in a large area involving the right olfactory and memory regions, with heightened activation specifically for sommeliers during an olfactory task. Our results indicate that sommeliers’ brains show specialization in the expected regions of the olfactory and memory networks, and also in regions important in integration of internal sensory stimuli and external cues. Overall, these differences suggest that specialized expertise and training might result in enhancements in the brain well into adulthood. This is particularly important given the regions involved, which are the first to be impacted by many neurodegenerative diseases

Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage

Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ¹³C of −44 to −58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of ¹³C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150–million year–old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation

Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage

Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ¹³C of −44 to −58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of ¹³C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150–million year–old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation

Deep-sea microbes as tools to refine the rules of innate immune pattern recognition.

The assumption of near-universal bacterial detection by pattern recognition receptors is a foundation of immunology. The limits of this pattern recognition concept, however, remain undefined. As a test of this hypothesis, we determined whether mammalian cells can recognize bacteria that they have never had the natural opportunity to encounter. These bacteria were cultivated from the deep Pacific Ocean, where the genus Moritella was identified as a common constituent of the culturable microbiota. Most deep-sea bacteria contained cell wall lipopolysaccharide (LPS) structures that were expected to be immunostimulatory, and some deep-sea bacteria activated inflammatory responses from mammalian LPS receptors. However, LPS receptors were unable to detect 80% of deep-sea bacteria examined, with LPS acyl chain length being identified as a potential determinant of immunosilence. The inability of immune receptors to detect most bacteria from a different ecosystem suggests that pattern recognition strategies may be defined locally, not globally.R01 AI093589 - NIAID NIH HHS; P30 DK034854 - NIDDK NIH HHS; U19 AI133524 - NIAID NIH HHS; R01 AI147314 - NIAID NIH HHS; R01 AI116550 - NIAID NIH HHS; R37 AI116550 - NIAID NIH HHS; R01 AI123820 - NIAID NIH HHSAccepted manuscrip

Mineralogy of Deep-Sea Coral Aragonites as a Function of Aragonite Saturation State

In an ocean with rapidly changing chemistry, studies have assessed coral skeletal health under projected ocean acidification (OA) scenarios by characterizing morphological distortions in skeletal architecture and measuring bulk properties, such as net calcification and dissolution. Few studies offer more detailed information on skeletal mineralogy. Since aragonite crystallography will at least partially govern the material properties of coral skeletons, such as solubility and strength, it is important to understand how it is influenced by environmental stressors. Here, we take a mineralogical approach using micro X-ray diffraction (XRD) and whole pattern Rietveld refinement analysis to track crystallographic shifts in deep-sea coral Lophelia pertusa samples collected along a natural seawater aragonite saturation state gradient (Ωsw = 1.15–1.44) in the Gulf of Mexico. Our results reveal statistically significant linear relationships between rising Ωsw and increasing unit cell volume driven by an anisotropic lengthening along the b-axis. These structural changes are similarly observed in synthetic aragonites precipitated under various saturation states, indicating that these changes are inherent to the crystallography of aragonite. Increased crystallographic disorder via widening of the full width at half maximum of the main (111) XRD peaks trend with increased Ba substitutions for Ca, however, trace substitutions by Ba, Sr, and Mg do not trend with crystal lattice parameters in our samples. Instead, we observe a significant trend of increasing calcite content as a function of both decreasing unit cell parameters as well as decreasing Ωsw. This may make calcite incorporation an important factor to consider in coral crystallography, especially under varying aragonite saturation states (ΩAr). Finally, by defining crystallography-based linear relationships between ΩAr of synthetic aragonite analogs and lattice parameters, we predict internal calcifying fluid saturation state (Ωcf = 11.1–17.3 calculated from b-axis lengths; 15.2–25.2 calculated from unit cell volumes) for L. pertusa, which may allow this species to calcify despite the local seawater conditions. This study will ideally pave the way for future studies to utilize quantitative XRD in exploring the impact of physical and chemical stressors on biominerals