Becker
Cynthia C.
Becker
Cynthia C.
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ArticleBenthic 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, AmyBenthic 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.
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ArticleImpact 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, AmyTropical 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.
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ArticleSoundscapes influence the settlement of the common caribbean coral porites astreoides irrespective of light conditions(Royal Society, 2018-12-12) Lillis, Ashlee ; Apprill, Amy ; Suca, Justin J. ; Becker, Cynthia ; Llopiz, Joel K. ; Mooney, T. AranThe settlement of reef-building corals is critical to the survival and recovery of reefs. Recent evidence indicates that coral larvae orient towards reef sound, yet the components of the acoustic environment that may attract coral larvae and induce settlement are unknown. Here we investigated the effects of ambient soundscapes on settlement of Porites astreoides coral larvae using in situ chambers on reefs differing in habitat quality (coral and fish abundance). Mean larval settlement was twice as high in an acoustic environment with high levels of low-frequency sounds, typical of a high-quality, healthy reef; this result was observed in both natural light and dark treatments. Overall, the enhancement of coral settlement by soundscapes typical of healthy reefs suggests a positive feedback where soundscape properties of reefs with elevated coral and fish abundance may facilitate coral recruitment.
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PreprintMicrobial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field-based sequencing approach(Society for Applied Microbiology, 2021-08-25) Becker, Cynthia ; Brandt, Marilyn ; Miller, Carolyn A. ; Apprill, AmyStony Coral Tissue Loss Disease (SCTLD) is a devastating disease. Since 2014, it has spread along the entire Florida Reef Tract and into the greater Caribbean. It was first detected in the United States Virgin Islands in January 2019. To more quickly identify microbial bioindicators of disease, we developed a rapid pipeline for microbiome sequencing. Over a span of 10 days we collected, processed and sequenced coral and near-coral seawater microbiomes from diseased and apparently healthy Colpophyllia natans, Montastraea cavernosa, Meandrina meandrites and Orbicella franksi. Analysis of bacterial and archaeal 16S ribosomal RNA gene sequences revealed 25 bioindicator amplicon sequence variants (ASVs) enriched in diseased corals. These bioindicator ASVs were additionally recovered in near-coral seawater (<5 cm of coral surface), a potential reservoir for pathogens. Phylogenetic analysis of microbial bioindicators with sequences from the Coral Microbiome Database revealed that Vibrio, Arcobacter, Rhizobiaceae and Rhodobacteraceae sequences were related to disease-associated coral bacteria and lineages novel to corals. Additionally, four ASVs (Algicola, Cohaesibacter, Thalassobius and Vibrio) were matches to microbes previously associated with SCTLD that should be targets for future research. Overall, this work suggests that a rapid sequencing framework paired with specialized databases facilitates identification of microbial disease bioindicators.
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ArticleMicrobial 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, AmyIn 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.
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ArticleExperimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue(Springer, 2022-05-30) Huntley, Naomi ; Brandt, Marilyn ; Becker, Cynthia ; Miller, Carolyn A. ; Meiling, Sonora S. ; Correa, Adrienne M.S. ; Holstein, Daniel M. ; Muller, Erinn ; Mydlarz, Laura ; Smith, Tyler B. ; Apprill, AmyStony coral tissue loss disease (SCTLD) is a widespread and deadly disease that affects nearly half of Caribbean coral species. To understand the microbial community response to this disease, we performed a disease transmission experiment on US Virgin Island (USVI) corals, exposing six species of coral with varying susceptibility to SCTLD. The microbial community of the surface mucus and tissue layers were examined separately using a small subunit ribosomal RNA gene-based sequencing approach, and data were analyzed to identify microbial community shifts following disease acquisition, potential causative pathogens, as well as compare microbiota composition to field-based corals from the USVI and Florida outbreaks. While all species displayed similar microbiome composition with disease acquisition, microbiome similarity patterns differed by both species and mucus or tissue microhabitat. Further, disease exposed but not lesioned corals harbored a mucus microbial community similar to those showing disease signs, suggesting that mucus may serve as an early warning detection for the onset of SCTLD. Like other SCTLD studies in Florida, Rhodobacteraceae, Arcobacteraceae, Desulfovibrionaceae, Peptostreptococcaceae, Fusibacter, Marinifilaceae, and Vibrionaceae dominated diseased corals. This study demonstrates the differential response of the mucus and tissue microorganisms to SCTLD and suggests that mucus microorganisms may be diagnostic for early disease exposure.
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ArticleMicrobial 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, SeanMicroorganisms 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.
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ThesisExamining coral reef ecosystem dynamics using microorganisms and metabolites(Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2023-06) Becker, Cynthia C. ; Apprill, AmyMicroorganisms and metabolites are foundational to the success and productivity of biodiverse and economically important coral reef ecosystems and are also tightly connected. Metabolites are small organic compounds produced by reef organisms and are the chemical currencies exchanged by unicellular microorganisms (bacteria and archaea) within the seawater. Although central to reef biogeochemical cycling, we still lack fundamental information on the dynamics of these components of reefs. In this dissertation, I analyzed microorganisms in Caribbean coral reef habitats over temporal, spatial and reef health gradients as well as metabolites in a spatial reef study. In Chapter 2, I applied a rapid sequencing methodology to corals afflicted with the lethal stony coral tissue loss disease and identified specific microorganisms which were biological indicators of the disease. In Chapter 3, I investigated the dynamics of microorganisms over short temporal tidal and diurnal cycles, as well as spatially across US Virgin Island (USVI) coastal habitats. In these habitats, I found tidal cycles were driving changes in microbial communities within mangroves, but diurnal patterns were more important in reef habitats. In Chapter 4, I examined reefs over a longer temporal scale by contributing to the building of a 7-year time-series of USVI reef ecology and found that reef water microorganisms were predictive of hurricane and stony coral tissue loss disease impacts. Finally, in Chapter 5, I combined analyses of untargeted and targeted metabolomics, microbial taxa, and functional genes from metagenomics across 300 km of reefs in Florida, in addition to microorganisms in healthy and diseased corals. With this unprecedented combination of ‘omics datasets, I found that biogeographic zones, environmental features, and underlying habitat characteristics were related to microbial and metabolite features in the reef ecosystem. Further, I identified microorganisms and metabolites which were characteristic of specific reef biogeographic zones. Collectively, my work advances our understanding into the dynamics of microorganisms and metabolites in biodiverse coral reef habitats across natural temporal and spatial gradients and in the face of unprecedented stress and disturbance.
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ArticleA meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in unaffected and lesion tissue in diseased colonies(Springer, 2023-03-09) Rosales, Stephanie M. ; Huebner, Lindsay K. ; Evans, James S. ; Apprill, Amy ; Baker, Andrew C. ; Becker, Cynthia C. ; Bellantuono, Anthony J. ; Brandt, Marilyn E. ; Clark, Abigail S. ; del Campo, Javier ; Dennison, Caroline E. ; Eaton, Katherine R. ; Huntley, Naomi E. ; Kellogg, Christina A. ; Medina, Mónica ; Meyer, Julie L. ; Muller, Erinn M. ; Rodriguez-Lanetty, Mauricio ; Salerno, Jennifer L. ; Schill, William B. ; Shilling, Erin N. ; Stewart, Julia Marie ; Voss, Joshua D.Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with the limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and colony health states (apparently healthy colony tissue (AH), and unaffected (DU) and lesion (DL) tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha-diversity between AH and DL was not different; however, DU showed increased alpha-diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. In DL, Rhodobacterales and Peptostreptococcales–Tissierellales were prominent in structuring microbial interactions. We also predict an enrichment of an alpha-toxin in DL samples which is typically found in Clostridia. We provide a consensus of SCTLD-associated bacteria prior to and during lesion formation and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.
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ArticleMicroorganisms 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, AmyAs 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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ArticleMicroorganisms uniquely capture and predict stony coral tissue loss disease and hurricane disturbance impacts on US Virgin Island reefs(Wiley, 2024-04-04) Becker, Cynthia C. ; Weber, Laura ; Llopiz, Joel K. ; Mooney, T. Aran ; Apprill, AmyCoral reef ecosystems are now commonly affected by major climate and disease disturbances. Disturbance impacts are typically recorded using reef benthic cover, but this may be less reflective of other ecosystem processes. To explore the potential for reef water-based disturbance indicators, we conducted a 7-year time series on US Virgin Island reefs where we examined benthic cover and reef water nutrients and microorganisms from 2016 to 2022, which included two major disturbances: hurricanes Irma and Maria in 2017 and the stony coral tissue loss disease outbreak starting in 2020. The disease outbreak coincided with the largest changes in the benthic habitat, with increases in the percent cover of turf algae and Ramicrusta, an invasive alga. While sampling timepoint contributed most to changes in reef water nutrient composition and microbial community beta diversity, both disturbances led to increases in ammonium concentration, a mechanism likely contributing to observed microbial community shifts. We identified 10 microbial taxa that were sensitive and predictive of increasing ammonium concentration. This included the decline of the oligotrophic and photoautotrophic Prochlorococcus and the enrichment of heterotrophic taxa. As disturbances impact reefs, the changing nutrient and microbial regimes may foster a type of microbialization, a process that hastens reef degradation.