Weber Laura

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Weber

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Laura

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0000-0003-4957-2758

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The coral ecosphere: a unique coral reef habitat that fosters coral-microbial interactions

(Wiley, 2019-05-21) Weber, Laura ; Gonzalez‐Díaz, Patricia ; Armenteros, Maickel ; Apprill, Amy

Scleractinian corals are bathed in a sea of planktonic and particle‐associated microorganisms. The metabolic products of corals influence the growth and composition of microorganisms, but interactions between corals and seawater microorganisms are underexplored. We conducted a field‐based survey to compare the biomass, diversity, composition, and functional capacity of microorganisms in small‐volume seawater samples collected adjacent to five coral species with seawater collected > 1 m away from the reef substrate on the same reefs. Seawater collected close to corals generally harbored copiotrophic‐type bacteria and its bacterial and archaeal composition was influenced by coral species as well as the local reef environment. Trends in picoplankton abundances were variable and either increased or decreased away from coral colonies based on coral species and picoplankton functional group. Genes characteristic of surface‐attached and potentially virulent microbial lifestyles were enriched in near‐coral seawater compared to reef seawater. There was a prominent association between the coral Porites astreoides and the coral symbiont Endozoicomonas, suggesting recruitment and/or shedding of these cells into the surrounding seawater. This evidence extends our understanding of potential species‐specific and reef site‐influenced microbial interactions that occur between corals and microorganisms within this near‐coral seawater environment that we propose to call the “coral ecosphere.” Microbial interactions that occur within the coral ecosphere could influence recruitment of coral‐associated microorganisms and facilitate the transfer of coral metabolites into the microbial food web, thus fostering reef biogeochemical cycling and a linkage between corals and the water column.
Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals

(Springer Nature, 2020-12-20) Babbin, Andrew ; Tamasi, Tyler ; Dumit, Diana ; Weber, Laura ; Rodríguez, María Victoria Iglesias ; Schwartz, Sarah L. ; Armenteros, Maickel ; Wankel, Scott D. ; Apprill, Amy

Coral reef health depends on an intricate relationship among the coral animal, photosynthetic algae, and a complex microbial community. The holobiont can impact the nutrient balance of their hosts amid an otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Here we use 15N-tracer experiments to produce the first simultaneous measurements of ammonium oxidation, nitrate reduction, and nitrous oxide (N2O) production among five iconic species of reef-building corals (Acropora palmata, Diploria labyrinthiformis, Orbicella faveolata, Porites astreoides, and Porites porites) in the highly protected Jardines de la Reina reefs of Cuba. Nitrate reduction is present in most species, but ammonium oxidation is low potentially due to photoinhibition and assimilatory competition. Coral-associated rates of N2O production indicate a widespread potential for denitrification, especially among D. labyrinthiformis, at rates of ~1 nmol cm−2 d−1. In contrast, A. palmata displays minimal active nitrogen metabolism. Enhanced rates of nitrate reduction and N2O production are observed coincident with dark net respiration periods. Genomes of bacterial cultures isolated from multiple coral species confirm that microorganisms with the ability to respire nitrate anaerobically to either dinitrogen gas or ammonium exist within the holobiont. This confirmation of anaerobic nitrogen metabolisms by coral-associated microorganisms sheds new light on coral and reef productivity.
Microbial signatures of protected and impacted Northern Caribbean reefs: changes from Cuba to the Florida Keys.

(Wiley, 2019-11-19) Weber, Laura ; Gonzalez‐Díaz, Patricia ; Armenteros, Maickel ; Ferrer, Víctor M. ; Bretos, Fernando ; Bartels, Erich ; Santoro, Alyson E. ; Apprill, Amy

There are a few baseline reef‐systems available for understanding the microbiology of healthy coral reefs and their surrounding seawater. Here, we examined the seawater microbial ecology of 25 Northern Caribbean reefs varying in human impact and protection in Cuba and the Florida Keys, USA, by measuring nutrient concentrations, microbial abundances, and respiration rates as well as sequencing bacterial and archaeal amplicons and community functional genes. Overall, seawater microbial composition and biogeochemistry were influenced by reef location and hydrogeography. Seawater from the highly protected ‘crown jewel’ offshore reefs in Jardines de la Reina, Cuba had low concentrations of nutrients and organic carbon, abundant Prochlorococcus, and high microbial community alpha diversity. Seawater from the less protected system of Los Canarreos, Cuba had elevated microbial community beta‐diversity whereas waters from the most impacted nearshore reefs in the Florida Keys contained high organic carbon and nitrogen concentrations and potential microbial functions characteristic of microbialized reefs. Each reef system had distinct microbial signatures and within this context, we propose that the protection and offshore nature of Jardines de la Reina may preserve the oligotrophic paradigm and the metabolic dependence of the community on primary production by picocyanobacteria.
Incubation experiments were conducted in St. John, US Virgin Islands to investigate the macronutrient drawdown response of reef seawater microbial communities to exudates released from the coral species Porites astreoides and Gorgonia ventalina.

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2022-11-10) Weber, Laura ; Apprill, Amy ; Kujawinski, Elizabeth

Incubation experiments were conducted in St. John, US Virgin Islands to investigate the composition of exudates released from different species of benthic organisms, and the response of reef seawater microbial communities to mixed exudates released from different species and to specific metabolites. Exudates were collected from the stony coral Porites astreoides, and the octocoral Gorgonia ventalina after an 8 hour incubation. Reef seawater microbial communities were incubated separately in the presence of exudates from P. astreoides and G. ventalina for 48 hours and samples were collected to monitor changes in macronutrient concentrations. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/865193
Incubation experiments were conducted in St. John, US Virgin Islands to investigate the response of reef seawater microbial communities to the mixed exudates released from the coral species Porites astreoides and Gorgonia ventalina.

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2022-11-10) Weber, Laura ; Apprill, Amy ; Kujawinski, Elizabeth

Incubation experiments were conducted in St. John, US Virgin Islands to investigate the composition of exudates released from different species of benthic organisms, and the response of reef seawater microbial communities to mixed exudates released from different species and to specific metabolites. Exudates were collected from the stony coral Porites astreoides, and the octocoral Gorgonia ventalina after an 8 hour incubation. Reef seawater microbial communities were incubated separately in the presence of exudates from P. astreoides and G. ventalina for 48 hours and samples were collected to monitor changes in microbial abundance via flow cytometry and microbial community composition via 16S rRNA gene sequencing. Complementary Targeted and Untargeted metabolomic data from these incubation experiments is available on the MetaboLights database under accession number MTBLS2855. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/865739
Benthic exometabolites and their ecological significance on threatened Caribbean coral reefs

(Springer, 2022-10-17) Weber, Laura ; Soule, Melissa Kido ; Longnecker, Krista ; Becker, Cynthia C. ; Huntley, Naomi ; Kujawinski, Elizabeth B. ; Apprill, Amy

Benthic organisms are the architectural framework supporting coral reef ecosystems, but their community composition has recently shifted on many reefs. Little is known about the metabolites released from these benthic organisms and how compositional shifts may influence other reef life, including prolific microorganisms. To investigate the metabolite composition of benthic exudates and their ecological significance for reef microbial communities, we harvested exudates from six species of Caribbean benthic organisms including stony corals, octocorals, and an invasive encrusting alga, and subjected these exudates to untargeted and targeted metabolomics approaches using liquid chromatography-mass spectrometry. Incubations with reef seawater microorganisms were conducted to monitor changes in microbial abundances and community composition using 16 S rRNA gene sequencing in relation to exudate source and three specific metabolites. Exudates were enriched in amino acids, nucleosides, vitamins, and indole-based metabolites, showing that benthic organisms contribute labile organic matter to reefs. Furthermore, exudate compositions were species-specific, and riboflavin and pantothenic acid emerged as significant coral-produced metabolites, while caffeine emerged as a significant invasive algal-produced metabolite. Microbial abundances and individual microbial taxa responded differently to exudates from stony corals and octocorals, demonstrating that exudate mixtures released from different coral species select for specific bacteria. In contrast, microbial communities did not respond to individual additions of riboflavin, pantothenic acid, or caffeine. This work indicates that recent shifts in benthic organisms alter exudate composition and likely impact microbial communities on coral reefs.
Incubation experiments were conducted in St. John, US Virgin Islands to investigate the response of reef seawater microbial communities to the specific metabolites riboflavin, pantothenic acid, and caffeine.

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2022-11-10) Weber, Laura ; Apprill, Amy ; Kujawinski, Elizabeth

Pre-filtered reef seawater microbial communities collected from Lameshur Bay, U.S. Virgin Islands were incubated separately in the presence of the individual metabolites riboflavin, pantothenic acid, and caffeine for 24 hours and samples were collected to monitor changes in microbial community composition using 16S rRNA gene sequencing and microbial abundances using flow cytometry. Targeted metabolomic data from these incubations is available on the MetaboLights database under accession number MTBLS3286. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/865159
Impact of prawn farming effluent on coral reef water nutrients and microorganisms

(Inter-Research, 2017-09-22) Becker, Cynthia ; Hughen, Konrad A. ; Mincer, Tracy J. ; Ossolinski, Justin E. ; Weber, Laura ; Apprill, Amy

Tropical coral reefs are characterized by low-nutrient waters that support oligotrophic picoplankton over a productive benthic ecosystem. Nutrient-rich effluent released from aquaculture facilities into coral reef environments may potentially upset the balance of these ecosystems by altering picoplankton dynamics. In this study, we examined how effluent from a prawn (Litopenaeus vannamei) farming facility in Al Lith, Saudi Arabia, impacted the inorganic nutrients and prokaryotic picoplankton community in the waters overlying coral reefs in the Red Sea. Across 24 sites, ranging 0-21 km from the effluent point source, we measured nutrient concentrations, quantified microbial cell abundances, and sequenced bacterial and archaeal small subunit ribosomal RNA (SSU rRNA) genes to examine picoplankton phylogenetic diversity and community composition. Our results demonstrated that sites nearest to the outfall had increased concentrations of phosphate and ammonium and elevated abundances of non-pigmented picoplankton (generally heterotrophic bacteria). Shifts in the composition of the picoplankton community were observed with increasing distance from the effluent canal outfall. Waters within 500 m of the outfall harbored the most distinct picoplanktonic community and contained putative pathogens within the genus Francisella and order Rickettsiales. While our study suggests that at the time of sampling, the Al Lith aquaculture facility exhibited relatively minor influences on inorganic nutrients and microbial communities, studying the longer-term impacts of the aquaculture effluent on the organisms within the reef will be necessary in order to understand the full extent of the facility’s impact on the reef ecosystem.
Extracellular reef metabolites across the protected Jardines de la Reina, Cuba Reef System

(Frontiers Media, 2020-12-14) Weber, Laura ; Armenteros, Maickel ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Apprill, Amy

Coral reef ecosystems are incredibly diverse marine biomes that rely on nutrient cycling by microorganisms to sustain high productivity in generally oligotrophic regions of the ocean. Understanding the composition of extracellular reef metabolites in seawater, the small organic molecules that serve as the currency for microorganisms, may provide insight into benthic-pelagic coupling as well as the complexity of nutrient cycling in coral reef ecosystems. Jardines de la Reina (JR), Cuba is an ideal environment to examine extracellular metabolites across protected and high-quality reefs. Here, we used liquid chromatography mass spectrometry (LC-MS) to quantify specific known metabolites of interest (targeted metabolomics approach) and to survey trends in metabolite feature composition (untargeted metabolomics approach) from surface and reef depth (6 – 14 m) seawater overlying nine forereef sites in JR. We found that untargeted metabolite feature composition was surprisingly similar between reef depth and surface seawater, corresponding with other biogeochemical and physicochemical measurements and suggesting that environmental conditions were largely homogenous across forereefs within JR. Additionally, we quantified 32 of 53 detected metabolites using the targeted approach, including amino acids, nucleosides, vitamins, and other metabolic intermediates. Two of the quantified metabolites, riboflavin and xanthosine, displayed interesting trends by depth. Riboflavin concentrations were higher in reef depth compared to surface seawater, suggesting that riboflavin may be produced by reef organisms at depth and degraded in the surface through photochemical oxidation. Xanthosine concentrations were significantly higher in surface reef seawater. 5′-methylthioadenosine (MTA) concentrations increased significantly within the central region of the archipelago, displaying biogeographic patterns that warrant further investigation. Here we lay the groundwork for future investigations of variations in metabolite composition across reefs, sources and sinks of reef metabolites, and changes in metabolites over environmental, temporal, and reef health gradients.
Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event

(Nature Publishing Group, 2016-12-07) Diaz, Julia M. ; Hansel, Colleen M. ; Apprill, Amy ; Brighi, Caterina ; Zhang, Tong ; Weber, Laura ; McNally, Sean ; Xun, Liping

The reactive oxygen species superoxide (O2·−) is both beneficial and detrimental to life. Within corals, superoxide may contribute to pathogen resistance but also bleaching, the loss of essential algal symbionts. Yet, the role of superoxide in coral health and physiology is not completely understood owing to a lack of direct in situ observations. By conducting field measurements of superoxide produced by corals during a bleaching event, we show substantial species-specific variation in external superoxide levels, which reflect the balance of production and degradation processes. Extracellular superoxide concentrations are independent of light, algal symbiont abundance and bleaching status, but depend on coral species and bacterial community composition. Furthermore, coral-derived superoxide concentrations ranged from levels below bulk seawater up to ∼120 nM, some of the highest superoxide concentrations observed in marine systems. Overall, these results unveil the ability of corals and/or their microbiomes to regulate superoxide in their immediate surroundings, which suggests species-specific roles of superoxide in coral health and physiology.
Marine mammal skin microbiotas are influenced by host phylogeny

(The Royal Society, 2020-05-20) Apprill, Amy ; Miller, Carolyn A. ; Van Cise, Amy M. ; U'Ren, Jana M. ; Leslie, Matthew S. ; Weber, Laura ; Baird, Robin W. ; Robbins, Jooke ; Landry, Scott ; Bogomolni, Andrea L. ; Waring, Gordon T.

Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai‘i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.
Optimization of DNA extraction for advancing coral microbiota investigations

(BioMed Central, 2017-02-08) Weber, Laura ; DeForce, Emelia A. ; Apprill, Amy

We designed a two-phase study in order to propose a comprehensive and efficient method for DNA extraction from microbial cells present in corals and investigate if extraction method influences microbial community composition. During phase I, total DNA was extracted from seven coral species in a replicated experimental design using four different MO BIO Laboratories, Inc., DNA Isolation kits: PowerSoil®, PowerPlant® Pro, PowerBiofilm®, and UltraClean® Tissue & Cells (with three homogenization permutations). Technical performance of the treatments was evaluated using DNA yield and amplification efficiency of small subunit ribosomal RNA (SSU ribosomal RNA (rRNA)) genes. During phase II, potential extraction biases were examined via microbial community analysis of SSU rRNA gene sequences amplified from the most successful DNA extraction treatments. In phase I of the study, the PowerSoil® and PowerPlant® Pro extracts contained low DNA concentrations, amplified poorly, and were not investigated further. Extracts from PowerBiofilm® and UltraClean® Tissue and Cells permutations were further investigated in phase II, and analysis of sequences demonstrated that overall microbial community composition was dictated by coral species and not extraction treatment. Finer pairwise comparisons of sequences obtained from Orbicella faveolata, Orbicella annularis, and Acropora humilis corals revealed subtle differences in community composition between the treatments; PowerBiofilm®-associated sequences generally had higher microbial richness and the highest coverage of dominant microbial groups in comparison to the UltraClean® Tissue and Cells treatments, a result likely arising from using a combination of different beads during homogenization. Both the PowerBiofilm® and UltraClean® Tissue and Cells treatments are appropriate for large-scale analyses of coral microbiota. However, studies interested in detecting cryptic microbial members may benefit from using the PowerBiofilm® DNA treatment because of the likely enhanced lysis efficiency of microbial cells attributed to using a variety of beads during homogenization. Consideration of the methodology involved with microbial DNA extraction is particularly important for studies investigating complex host-associated microbiota.
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton

(Inter-Research, 2015-06-04) Apprill, Amy ; McNally, Sean ; Parsons, Rachel ; Weber, Laura

High-throughput sequencing of small subunit ribosomal RNA (SSU rRNA) genes from marine environments is a widely applied method used to uncover the composition of microbial communities. We conducted an analysis of surface ocean waters with the commonly employed hypervariable 4 region SSU rRNA gene primers 515F and 806R, and found that bacteria belonging to the SAR11 clade of Alphaproteobacteria, a group typically making up 20 to 40% of the bacterioplankton in this environment, were greatly underrepresented and comprised <4% of the total community. Using the SILVA reference database, we found a single nucleotide mismatch to nearly all SAR11 subclades, and revised the 806R primer so that it increased the detection of SAR11 clade sequences in the database from 2.6 to 96.7%. We then compared the performance of the original and revised 806R primers in surface seawater samples, and found that SAR11 comprised 0.3 to 3.9% of sequences with the original primers and 17.5 to 30.5% of the sequences with the revised 806R primer. Furthermore, an investigation of seawater obtained from aquaria revealed that SAR11 sequences acquired with the revised 806R primer were more similar to natural cellular abundances of SAR11 detected using fluorescence in situ hybridization counts. Collectively, these results demonstrate that a minor adjustment to the 806R primer will greatly increase detection of the globally abundant SAR11 clade in marine and lake environments, and enable inclusion of this important bacterial lineage in experimental and environmental-based studies.
Microbial and nutrient dynamics in mangrove, reef, and seagrass waters over tidal and diurnal time scales

(Inter Research, 2020-10-08) Becker, Cynthia ; Weber, Laura ; Suca, Justin J. ; Llopiz, Joel K. ; Mooney, T. Aran ; Apprill, Amy

In coral reefs and adjacent seagrass meadow and mangrove environments, short temporal scales (i.e. tidal, diurnal) may have important influences on ecosystem processes and community structure, but these scales are rarely investigated. This study examines how tidal and diurnal forcings influence pelagic microorganisms and nutrient dynamics in 3 important and adjacent coastal biomes: mangroves, coral reefs, and seagrass meadows. We sampled for microbial (Bacteria and Archaea) community composition, cell abundances and environmental parameters at 9 coastal sites on St. John, US Virgin Islands that spanned 4 km in distance (4 coral reefs, 2 seagrass meadows and 3 mangrove locations within 2 larger bays). Eight samplings occurred over a 48 h period, capturing day and night microbial dynamics over 2 tidal cycles. The seagrass and reef biomes exhibited relatively consistent environmental conditions and microbial community structure but were dominated by shifts in picocyanobacterial abundances that were most likely attributed to diel dynamics. In contrast, mangrove ecosystems exhibited substantial daily shifts in environmental parameters, heterotrophic cell abundances and microbial community structure that were consistent with the tidal cycle. Differential abundance analysis of mangrove-associated microorganisms revealed enrichment of pelagic oligotrophic taxa during high tide and enrichment of putative sediment-associated microbes during low tide. Our study underpins the importance of tidal and diurnal time scales in structuring coastal microbial and nutrient dynamics, with diel and tidal cycles contributing to a highly dynamic microbial environment in mangroves, and time of day likely contributing to microbial dynamics in seagrass and reef biomes.
Small-scale variability dominates benthic coverage and diversity across the Jardines de la Reina, Cuba coral reef system

(Frontiers Media, 2019-11-29) Hernández-Fernández, Leslie ; González de Zayas, Roberto ; Weber, Laura ; Apprill, Amy ; Armenteros, Maickel

Coral reefs are complex and biodiverse ecosystems that are undergoing significant change. Understanding reef composition and biodiversity at multiple spatial scales is necessary to track both large-scale and more subtle ecosystem changes. The Jardines de la Reina (JR) archipelago, located offshore of the island of Cuba, contains the largest marine protected area (MPA) in the Caribbean Sea but lacks multi-scale studies. In this contribution, we documented the diversity of scleractinian corals, octocorals, algae, and sponges across nested spatial scales spanning four orders of magnitude (101–105 m). In addition, we tested the hypothesis that species diversity followed a gradient along the ca. 200 km of reef tract. Across the archipelago, we examined benthic cover and species diversity within 255 photo-quadrats (25 × 25 cm) at 13 fore reef sites (two sampling locations per site, and 10 photo-quadrats per location). Small-scale (101 m) variability between photo-quadrats characterized the coral reef community structure in JR compared with local- (102 m) and mesoscale (104–105 m) variability. This finding suggests that biological processes (e.g., recruitment, competition) had primacy over hydrodynamics for driving the differences in reef community composition. However, the dominance of algae and low cover and diversity of scleractinian corals suggests the pervasive effects of global change on coral communities despite potential benefits provided by the MPA (e.g., oligotrophy and abundance of herbivores). There was no gradient of benthic community structure along the fore reef tract of JR; instead, a patchy distribution occurred in response to more subtle drivers acting at local scales. Overall, our multi-scale comparison was useful for differentiating the impacts of processes potentially impacting the JR reefs, thus providing important information to understand how reef communities are impacted by different environmental and anthropogenic stressors, and the potential benefits of MPAs.
Diel, daily, and spatial variation of coral reef seawater microbial communities

(Public Library of Science, 2020-03-11) Weber, Laura ; Apprill, Amy

Reef organisms influence microorganisms within the surrounding seawater, yet the spatial and temporal dynamics of seawater microbial communities located in proximity to corals are rarely investigated. To better understand reef seawater microbial community dynamics over time and space, we collected small-volume seawater samples during the day and night over a 72 hour period from three locations that differed in spatial distance from 5 Porites astreoides coral colonies on a shallow reef in St. John, U.S. Virgin Islands: near-coral (sampled 5 cm horizontally from each colony), reef-depth (sampled 2 m above each colony) and surface seawater (sampled 1 m from the seawater surface). At all time points and locations, we quantified abundances of microbial cells, sequenced small subunit rRNA genes of bacterial and archaeal communities, and measured inorganic nutrient concentrations. Prochlorococcus and Synechococcus cells were consistently elevated at night compared to day and these abundances changed over time, corresponding with temperature, nitrite, and silicate concentrations. During the day, bacterial and archaeal alpha diversity was significantly higher in reef-depth and near-coral seawater compared to the surface seawater, signifying that the reef influences the diversity of the seawater microorganisms. At night, alpha diversity decreased across all samples, suggesting that photosynthesis may favor a more taxonomically diverse community. While Prochlorococcus exhibited consistent temporal rhythmicity, additional taxa were enriched in reef seawater at night compared to day or in reef-depth compared to surface seawater based on their normalized sequence counts. There were some significant differences in nutrient concentrations and cell abundances between reef-depth and near-coral seawater but no clear trends. This study demonstrates that temporal variation supersedes small-scale spatial variation in proximity to corals in reef seawater microbial communities. As coral reefs continue to change in benthic composition worldwide, monitoring microbial composition in response to temporal changes and environmental fluctuations will help discern normal variability from longer lasting changes attributed to anthropogenic stressors and global climate change.
Microbial ecology of coral-dominated reefs in the Federated States of Micronesia

(Inter Research, 2021-04-22) Apprill, Amy ; Holm, Henry C. ; Santoro, Alyson E. ; Becker, Cynthia ; Neave, Matthew J. ; Hughen, Konrad A. ; Richards Donà, Angela ; Aeby, Greta S. ; Work, Thierry M. ; Weber, Laura ; McNally, Sean

Microorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km2. On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (>85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features.
Characterizing the ecology of coral reef microorganisms across different scales within the Caribbean

(Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2020-02) Weber, Laura

Microorganisms sustain the high productivity of coral reefs and support one of the most diverse, valuable, and threatened ecosystems on Earth. Despite the importance of reef microorganisms, there is a lack of understanding about their ecology, especially on Caribbean reefs. Furthermore, the hastening degradation of reefs due to anthropogenic stressors has made it difficult to understand natural patterns in microbial communities in the context of larger-scale ecosystem changes. Using genomics and metabolomics approaches paired with biogeochemical and physicochemical measurements as well as quantification of cell abundances, this dissertation provides optimized methods for studying the coral microbiome, investigates potential interactions between corals and seawater microorganisms, measures changes in the composition and diversity of reef seawater microorganisms over different spatial and temporal scales, and provides baseline information about microbial ecology, biogeochemistry, and metabolite compositions of a protected and relatively-healthy Cuban coral reef-system to fill these critical knowledge gaps. I found that coral species and reef location influenced the composition of bacteria and archaea within the seawater surrounding coral colonies and this seawater was enriched with microbial colonization and interaction genes, providing evidence of a distinct microbial environment surrounding corals named the coral ecosphere. In a separate study, diel and daily variation superseded spatial variation in terms of influencing shifts in the microbial community. At a larger scale, seawater microbial communities collected from the protected reefsystem of Jardines de la Reina, Cuba had higher alpha diversity and community similarity, lower nutrient concentrations, and higher abundances of picocyanobacteria compared to less protected reef-systems within Los Canarreos, Cuba and the Florida Keys, U.S.A and seawater microbial communities collected from each reef-system were influenced by hydrogeography and environmental gradients. Lastly, the extracellular metabolite composition of reef seawater collected across Jardines de la Reina was highly similar, suggesting homogenous environmental and hydrogeographic conditions across these forereefs. Overall, this dissertation characterizes reef seawater microbial communities across different scales and provides novel, baseline information about a protected and understudied Cuban reef-system, offering critical information about the ecology of reef microorganisms within the Caribbean.
Biogeochemistry, metabolomics, and metagenomics of Florida's Coral Reef from sampling conducted over 15 days in June 2019

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2023-03-08) Apprill, Amy ; Kujawinski, Elizabeth ; Muller, Erinn ; Sandin, Stuart ; Weber, Laura ; Clark, Abigail ; Kido Soule, Melissa C. ; Longnecker, Krista ; Zgliczynski, Brian ; Sullivan, Chris ; Becker, Cynthia Carroll

This comparative 'omics dataset was collected over 15 days in June 2019 along Florida's Coral Reef. We assessed 85 reefs for the prevalence of stony coral tissue loss disease (SCTLD), nutrients (total organic carbon (TOC), total organic nitrogen (TON), inorganic nutrients), and abundances of microbial functional groups (Prochlorococcus, Synechococcus, picoeukaryotes, and heterotrophic microbes (unpigmented bacteria and archaea)), from reef depth waters. At 45 of the reefs, high-resolution photomosaics were used to examine the composition of benthic organisms. At 13 geographically dispersed reefs, we collected seawater (1.7 liters in biological triplicates) for both targeted and untargeted metabolomics analyses. Seawater (2 liters in duplicate) was collected at 26 sites, including the 13 examined for metabolomics, for taxonomic (bacteria and archaea 16S ribosomal RNA gene) and functional (shotgun metagenome) microbiome analyses, and chlorophyll. Given the stony coral tissue loss disease outbreak, we also targeted healthy and diseased coral tissue and near-coral seawater for taxonomic microbiome (16S rRNA gene) analysis (11 sites). Significance: Microorganisms and the dissolved metabolites they process are central to the functioning of ocean ecosystems. These 'invisible' ocean components are poorly understood in biodiverse and productive coral reef ecosystems, where they contribute to nutrient cycling and signaling cues between reef organisms. Microbes and dissolved metabolites offer a new means to examine reef features and have applications for conservation, monitoring, and restoration efforts in these changing ecosystems. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/890979
Microorganisms and dissolved metabolites distinguish Florida’s Coral Reef habitats

(National Academy of Sciences, 2023-09-05) Becker, Cynthia C. ; Weber, Laura ; Zgliczynski, Brian J. ; Sullivan, Chris ; Sandin, Stuart A. ; Muller, Erinn ; Clark, Abigail S. ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth ; Apprill, Amy

As coral reef ecosystems experience unprecedented change, effective monitoring of reef features supports management, conservation, and intervention efforts. Omic techniques show promise in quantifying key components of reef ecosystems including dissolved metabolites and microorganisms that may serve as invisible sensors for reef ecosystem dynamics. Dissolved metabolites are released by reef organisms and transferred among microorganisms, acting as chemical currencies and contributing to nutrient cycling and signaling on reefs. Here, we applied four omic techniques (taxonomic microbiome via amplicon sequencing, functional microbiome via shotgun metagenomics, targeted metabolomics, and untargeted metabolomics) to waters overlying Florida's Coral Reef, as well as microbiome profiling on individual coral colonies from these reefs to understand how microbes and dissolved metabolites reflect biogeographical, benthic, and nutrient properties of this 500-km barrier reef. We show that the microbial and metabolite omic approaches each differentiated reef habitats based on geographic zone. Further, seawater microbiome profiling and targeted metabolomics were significantly related to more reef habitat characteristics, such as amount of hard and soft coral, compared to metagenomic sequencing and untargeted metabolomics. Across five coral species, microbiomes were also significantly related to reef zone, followed by species and disease status, suggesting that the geographic water circulation patterns in Florida also impact the microbiomes of reef builders. A combination of differential abundance and indicator species analyses revealed metabolite and microbial signatures of specific reef zones, which demonstrates the utility of these techniques to provide new insights into reef microbial and metabolite features that reflect broader ecosystem processes.

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