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Alyson
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Alyson
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ArticleNitrogen cycling in the secondary nitrite maximum of the eastern tropical North Pacific off Costa Rica(John Wiley & Sons, 2015-12-15) Buchwald, Carolyn ; Santoro, Alyson E. ; Stanley, Rachel H. R. ; Casciotti, Karen L.Nitrite is a central intermediate in the marine nitrogen cycle and represents a critical juncture where nitrogen can be reduced to the less bioavailable N2 gas or oxidized to nitrate and retained in a more bioavailable form. We present an analysis of rates of microbial nitrogen transformations in the oxygen deficient zone (ODZ) within the eastern tropical North Pacific Ocean (ETNP). We determined rates using a novel one-dimensional model using the distribution of nitrite and nitrate concentrations, along with their natural abundance nitrogen (N) and oxygen (O) isotope profiles. We predict rate profiles for nitrate reduction, nitrite reduction, and nitrite oxidation throughout the ODZ, as well as the contributions of anammox to nitrite reduction and nitrite oxidation. Nitrate reduction occurs at a maximum rate of 25 nM d−1 at the top of the ODZ, at the same depth as the maximum rate of nitrite reduction, 15 nM d−1. Nitrite oxidation occurs at maximum rates of 10 nM d−1 above the secondary nitrite maximum, but also in the secondary nitrite maximum, within the ODZ. Anammox contributes to nitrite oxidation within the ODZ but cannot account for all of it. Nitrite oxidation within the ODZ that is not through anammox is also supported by microbial gene abundance profiles. Our results suggest the presence of nitrite oxidation within the ETNP ODZ, with implications for the distribution and physiology of marine nitrite-oxidizing bacteria, and for total nitrogen loss in the largest marine ODZ.
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ArticleThaumarchaeal ecotype distributions across the equatorial Pacific Ocean and their potential roles in nitrification and sinking flux attenuation(John Wiley & Sons, 2017-04-05) Santoro, Alyson E. ; Saito, Mak A. ; Goepfert, Tyler J. ; Lamborg, Carl H. ; Dupont, Christopher L. ; DiTullio, Giacomo R.Thaumarchaea are among the most abundant microbial groups in the ocean, but controls on their abundance and the distribution and metabolic potential of different subpopulations are poorly constrained. Here, two ecotypes of ammonia-oxidizing thaumarchaea were quantified using ammonia monooxygenase (amoA) genes across the equatorial Pacific Ocean. The shallow, or water column “A” (WCA), ecotype was the most abundant ecotype at the depths of maximum nitrification rates, and its abundance correlated with other biogeochemical indicators of remineralization such as NO3 : Si and total Hg. Metagenomes contained thaumarchaeal genes encoding for the catalytic subunit of the urease enzyme (ureC) at all depths, suggesting that members of both WCA and the deep, water column “B” (WCB) ecotypes may contain ureC. Coupled urea hydrolysis-ammonia oxidation rates were similar to ammonia oxidation rates alone, suggesting that urea could be an important source of ammonia for mesopelagic ammonia oxidizers. Potential inducement of metal limitation of both ammonia oxidation and urea hydrolysis was demonstrated via additions of a strong metal chelator. The water column inventory of WCA was correlated with the depth-integrated abundance of WCB, with both likely controlled by the flux of sinking particulate organic matter, providing strong evidence of vertical connectivity between the ecotypes. Further, depth-integrated amoA gene abundance and nitrification rates were correlated with particulate organic nitrogen flux measured by contemporaneously deployed sediment traps. Together, the results refine our understanding of the controls on thaumarchaeal distributions in the ocean, and provide new insights on the relationship between material flux and microbial communities in the mesopelagic.
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ArticleMicrobial 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, AmyThere 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.
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ArticleComplete genome sequences of two phylogenetically distinct Nitrospina strains isolated from the Atlantic and Pacific Oceans(American Society for Microbiology, 2022-05-02) Bayer, Barbara ; Kellom, Matthew ; Valois, Frederica ; Waterbury, John B. ; Santoro, Alyson E.The complete genome sequences of two chemoautotrophic nitrite-oxidizing bacteria of the genus Nitrospina are reported. Nitrospina gracilis strain Nb-211 was isolated from the Atlantic Ocean, and Nitrospina sp. strain Nb-3 was isolated from the Pacific Ocean. We report two highly similar ~3.07-Mbp genome sequences that differ by the presence of ferric iron chelator (siderophore) biosynthesis genes.
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ArticleOxygen isotopic composition of nitrate and nitrite produced by nitrifying cocultures and natural marine assemblages(Association for the Sciences of Limnology and Oceanography, 2012-09) Buchwald, Carolyn ; Santoro, Alyson E. ; McIlvin, Matthew R. ; Casciotti, Karen L.The δ18O value of nitrate produced during nitrification (δ18ONO3,nit) was measured in experiments designed to mimic oceanic conditions, involving cocultures of ammonia-oxidizing bacteria or ammonia-oxidizing archaea and nitrite-oxidizing bacteria, as well as natural marine assemblages. The estimates of ranged from −1.5‰ ± 0.1‰ to +1.3‰ ± 1.4‰ at δ18O values of water (H2O) and dissolved oxygen (O2) of 0‰ and 24.2‰ vs. Vienna Standard Mean Ocean Water, respectively. Additions of 18O-enriched H2O allowed us to evaluate the effects of oxygen (O) isotope fractionation and exchange on . Kinetic isotope effects for the incorporation of O atoms were the most important factors for setting overall values relative to the substrates (O2 and H2O). These isotope effects ranged from +10‰ to +22‰ for ammonia oxidation (O2 plus H2O incorporation) and from +1‰ to +27‰ for incorporation of H2O during nitrite oxidation. values were also affected by the amount and duration of nitrite accumulation, which permitted abiotic O atom exchange between nitrite and H2O. Coculture incubations where ammonia oxidation and nitrite oxidation were tightly coupled showed low levels of nitrite accumulation and exchange (3% ± 4%). These experiments had values of −1.5‰ to +0.7‰. Field experiments had greater accumulation of nitrite and a higher amount of exchange (22% to 100%), yielding an average value of +1.9‰ ± 3.0‰. Low levels of biologically catalyzed exchange in coculture experiments may be representative of nitrification in much of the ocean where nitrite accumulation is low. Abiotic oxygen isotope exchange may be important where nitrite does accumulate, such as oceanic primary and secondary nitrite maxima.
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ArticleMicrobial functional diversity across biogeochemical provinces in the central Pacific Ocean(National Academy of Sciences, 2022-09-13) Saunders, Jaclyn K. ; McIlvin, Matthew R. ; Dupont, Christopher L. ; Kaul, Drishti ; Moran, Dawn M. ; Horner, Tristan J. ; Laperriere, Sarah ; Webb, Eric A. ; Bosak, Tanja ; Santoro, Alyson E. ; Saito, Mak A.Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.
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ArticleMultifaceted impacts of the stony coral Porites astreoides on picoplankton abundance and community composition(John Wiley & Sons, 2016-10-12) McNally, Sean ; Parsons, Rachel J. ; Santoro, Alyson E. ; Apprill, AmyPicoplankton foster essential recycling of nutrients in the oligotrophic waters sustaining coral reef ecosystems. Despite this fact, there is a paucity of data on how the specific interactions between corals and planktonic bacteria and archaea (picoplankton) contribute to nutrient dynamics and reef productivity. Here, we utilized mesocosm experiments to investigate how corals and coral mucus influence picoplankton and nutrients in reef waters. Over 12 days, we tracked nutrient concentrations, picoplankton abundances and taxonomic composition of picoplankton using direct cell-counts, sequencing of SSU rRNA genes and fluorescent in situ hybridization-based abundances of dominant lineages in the presence or absence of Porites astreoides corals and with mucus additions. Our results demonstrate that when corals are present, Synechococcus, SAR11 and Rhodobacteraceae cells are preferentially removed. When corals were removed, their exudates enhanced the growth of diverse picoplankton, including SAR11 and Rhodobacteraceae. A seven-fold increase in nitrate concentration, possibly caused by nitrogen remineralization (ammonification coupled to nitrification) within the coral holobiont, may have further facilitated the growth of these taxa. In contrast, the addition of mucus resulted in rapid initial growth of total picoplankton and Rhodobacteraceae, but no measurable change in overall community structure. This study presents evidence of the multifaceted influences of corals on picoplankton, in which the coral holobiont selectively removes and promotes the growth of diverse picoplankton and remineralizes nitrogen.
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ArticleMetabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions(Springer Nature, 2020-11-23) Bayer, Barbara ; Saito, Mak A. ; McIlvin, Matthew R. ; Lücker, Sebastian ; Moran, Dawn M. ; Lankiewicz, Thomas S. ; Dupont, Christopher L. ; Santoro, Alyson E.The genus Nitrospira is the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T was isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential of N. marina based on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolved pCO2, and requires exogenous vitamin B12. In addition, N. marina is able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response of N. marina to low (∼5.6 µM) O2 concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinity cbb3-type terminal oxidase increased under O2 limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2 conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.
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ArticleAn intercomparison of oceanic methane and nitrous oxide measurements(Copernicus Publications on behalf of the European Geosciences Union, 2018-10-05) Wilson, Samuel T. ; Bange, Hermann W. ; Arévalo-Martínez, Damian L. ; Barnes, Jonathan ; Borges, Alberto V. ; Brown, Ian ; Bullister, John L. ; Burgos, Macarena ; Capelle, David W. ; Casso, Michael A. ; de la Paz, Mercedes ; Farías, Laura ; Fenwick, Lindsay ; Ferrón, Sara ; Garcia, Gerardo ; Glockzin, Michael ; Karl, David M. ; Kock, Annette ; Laperriere, Sarah ; Law, Cliff S. ; Manning, Cara C. ; Marriner, Andrew ; Myllykangas, Jukka-Pekka ; Pohlman, John W. ; Rees, Andrew P. ; Santoro, Alyson E. ; Tortell, Philippe D. ; Upstill-Goddard, Robert C. ; Wisegarver, David P. ; Zhang, Gui-Ling ; Rehder, GregorLarge-scale climatic forcing is impacting oceanic biogeochemical cycles and is expected to influence the water-column distribution of trace gases, including methane and nitrous oxide. Our ability as a scientific community to evaluate changes in the water-column inventories of methane and nitrous oxide depends largely on our capacity to obtain robust and accurate concentration measurements that can be validated across different laboratory groups. This study represents the first formal international intercomparison of oceanic methane and nitrous oxide measurements whereby participating laboratories received batches of seawater samples from the subtropical Pacific Ocean and the Baltic Sea. Additionally, compressed gas standards from the same calibration scale were distributed to the majority of participating laboratories to improve the analytical accuracy of the gas measurements. The computations used by each laboratory to derive the dissolved gas concentrations were also evaluated for inconsistencies (e.g., pressure and temperature corrections, solubility constants). The results from the intercomparison and intercalibration provided invaluable insights into methane and nitrous oxide measurements. It was observed that analyses of seawater samples with the lowest concentrations of methane and nitrous oxide had the lowest precisions. In comparison, while the analytical precision for samples with the highest concentrations of trace gases was better, the variability between the different laboratories was higher: 36% for methane and 27% for nitrous oxide. In addition, the comparison of different batches of seawater samples with methane and nitrous oxide concentrations that ranged over an order of magnitude revealed the ramifications of different calibration procedures for each trace gas. Finally, this study builds upon the intercomparison results to develop recommendations for improving oceanic methane and nitrous oxide measurements, with the aim of precluding future analytical discrepancies between laboratories.
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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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ArticleAn operational overview of the EXport Processes in the Ocean from RemoTe Sensing (EXPORTS) Northeast Pacific field deployment(University of California Press, 2021-07-07) Siegel, David A. ; Cetinić, Ivona ; Graff, Jason R. ; Lee, Craig M. ; Nelson, Norman B. ; Perry, Mary J. ; Soto Ramos, Inia ; Steinberg, Deborah K. ; Buesseler, Ken O. ; Hamme, Roberta C. ; Fassbender, Andrea ; Nicholson, David P. ; Omand, Melissa M. ; Robert, Marie ; Thompson, Andrew F. ; Amaral, Vinicius ; Behrenfeld, Michael J. ; Benitez-Nelson, Claudia R. ; Bisson, Kelsey ; Boss, Emmanuel S. ; Boyd, Philip ; Brzezinski, Mark A. ; Buck, Kristen N. ; Burd, Adrian B. ; Burns, Shannon ; Caprara, Salvatore ; Carlson, Craig A. ; Cassar, Nicolas ; Close, Hilary G. ; D'Asaro, Eric A. ; Durkin, Colleen A. ; Erickson, Zachary K. ; Estapa, Margaret L. ; Fields, Erik ; Fox, James ; Freeman, Scott ; Gifford, Scott M. ; Gong, Weida ; Gray, Deric ; Guidi, Lionel ; Haëntjens, Nils ; Halsey, Kim ; Huot, Yannick ; Hansell, Dennis A. ; Jenkins, Bethany D. ; Karp-Boss, Lee ; Kramer, Sasha J. ; Lam, Phoebe J. ; Lee, Jong-Mi ; Maas, Amy E. ; Marchal, Olivier ; Marchetti, Adrian ; McDonnell, Andrew M. P. ; McNair, Heather ; Menden-Deuer, Susanne ; Morison, Francoise ; Niebergall, Alexandria K. ; Passow, Uta ; Popp, Brian N. ; Potvin, Geneviève ; Resplandy, Laure ; Roca-Martí, Montserrat ; Roesler, Collin S. ; Rynearson, Tatiana A. ; Traylor, Shawnee ; Santoro, Alyson E. ; Seraphin, Kanesa ; Sosik, Heidi M. ; Stamieszkin, Karen ; Stephens, Brandon M. ; Tang, Weiyi ; Van Mooy, Benjamin ; Xiong, Yuanheng ; Zhang, XiaodongThe goal of the EXport Processes in the Ocean from RemoTe Sensing (EXPORTS) field campaign is to develop a predictive understanding of the export, fate, and carbon cycle impacts of global ocean net primary production. To accomplish this goal, observations of export flux pathways, plankton community composition, food web processes, and optical, physical, and biogeochemical (BGC) properties are needed over a range of ecosystem states. Here we introduce the first EXPORTS field deployment to Ocean Station Papa in the Northeast Pacific Ocean during summer of 2018, providing context for other papers in this special collection. The experiment was conducted with two ships: a Process Ship, focused on ecological rates, BGC fluxes, temporal changes in food web, and BGC and optical properties, that followed an instrumented Lagrangian float; and a Survey Ship that sampled BGC and optical properties in spatial patterns around the Process Ship. An array of autonomous underwater assets provided measurements over a range of spatial and temporal scales, and partnering programs and remote sensing observations provided additional observational context. The oceanographic setting was typical of late-summer conditions at Ocean Station Papa: a shallow mixed layer, strong vertical and weak horizontal gradients in hydrographic properties, sluggish sub-inertial currents, elevated macronutrient concentrations and low phytoplankton abundances. Although nutrient concentrations were consistent with previous observations, mixed layer chlorophyll was lower than typically observed, resulting in a deeper euphotic zone. Analyses of surface layer temperature and salinity found three distinct surface water types, allowing for diagnosis of whether observed changes were spatial or temporal. The 2018 EXPORTS field deployment is among the most comprehensive biological pump studies ever conducted. A second deployment to the North Atlantic Ocean occurred in spring 2021, which will be followed by focused work on data synthesis and modeling using the entire EXPORTS data set.