Distribution of nitrogen-cycling genes in an oxygen-depleted cyclonic eddy in the Alfonso Basin, Gulf of California
Ramiro Ramos-de la Cruz A B , Silvia Pajares
B C , Martín Merino-Ibarra B , María Adela Monreal-Gómez B and Erik Coria-Monter B
+ Author Affiliations
- Author Affiliations
A Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, Mexico City, 04510, Mexico.
B Unidad Académica de Ecología y Biodiversidad Acuática, Instituto de Ciencias del Mar y Limnología (ICML), Circuito exterior s/n, Ciudad Universitaria, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico.
C Corresponding author. Email: spajares@cmarl.unam.mx
Marine and Freshwater Research 72(8) 1173-1184 https://doi.org/10.1071/MF20074
Submitted: 11 March 2020 Accepted: 27 January 2021 Published: 16 March 2021
Abstract
The marine N cycle is driven mainly by microorganisms whose distribution can be shaped by mesoscale eddies. Recently, eddies containing oxygen minimum zones (OMZs) have been recognised as N-loss hotspots, complicating even more the calculations of the marine N budgets. As a contribution to this understanding, we investigated the effect of a cyclonic eddy confined in an oxygen-depleted basin on the distribution of the N-cycling communities. We measured hydrographic properties of the water column, nutrient concentrations, and the abundance of key genes involved in the processes of nitrification (archaeal and bacterial amoA), denitrification (nirS and nirK), dissimilatory nitrate reduction to ammonia (DNRA; nrfA) and anammox (hzo) within the eddy. Our results indicated that the cyclonic circulation affected the distribution of nutrients and the abundance of amoA and nirS genes, whereas oxygen influenced the distribution of nirK, nrfA, and hzo genes. Additionally, the aerobic ammonium oxidation by archaea seems to be an important source of nitrite, which might fuel denitrifier, DNRA, and anammox communities in this basin. These findings along with the high N deficit in the OMZ suggest the existence of an active N cycling that might enhance the N-loss in this oxygen-depleted basin.
Keywords: nitrogen deficit, N gene distribution, cyclonic circulation, OMZ, qPCR.
References
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.| A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |
Altabet, M. A., Ryabenko, E., Stramma, L., Wallace, D. W. R., Frank, M., Grasse, P., and Lavik, G. (2012). An eddy-stimulated hotspot for fixed nitrogen-loss from the Peru oxygen minimum zone. Biogeosciences 9, 4897–4908.
| An eddy-stimulated hotspot for fixed nitrogen-loss from the Peru oxygen minimum zone.Crossref | GoogleScholarGoogle Scholar |
Baith, K., Lindsay, R., Fu, G., and McClain, C. R. (2001). SeaDAS, a data analysis system for ocean-color satellite sensors. EoS 82, 202.
| SeaDAS, a data analysis system for ocean-color satellite sensors.Crossref | GoogleScholarGoogle Scholar |
Baltar, F., Arístegui, J., Gasol, J. M., Lekunberri, I., and Herndl, G. J. (2010). Mesoscale eddies: hotspots of prokaryotic activity and differential community structure in the ocean. The ISME Journal 4, 975–988.
| Mesoscale eddies: hotspots of prokaryotic activity and differential community structure in the ocean.Crossref | GoogleScholarGoogle Scholar | 20357833PubMed |
Bange, H. W., Rapsomanikis, S., and Andreae, M. O. (2001). Nitrous oxide cycling in the Arabian Sea. Journal of Geophysical Research. Oceans 106, 1053–1065.
| Nitrous oxide cycling in the Arabian Sea.Crossref | GoogleScholarGoogle Scholar |
Beman, J. M., Popp, B. N., and Francis, C. A. (2008). Molecular and biogeochemical evidence for ammonia oxidation by marine crenarchaeota in the Gulf of California. The ISME Journal 2, 429–441.
| Molecular and biogeochemical evidence for ammonia oxidation by marine crenarchaeota in the Gulf of California.Crossref | GoogleScholarGoogle Scholar | 18200070PubMed |
Bourbonnais, A., Altabet, M. A., Charoenpong, C. N., Larkum, J., Hu, H., Bange, H. W., and Stramma, L. (2015). N-loss isotope effects in the Peru oxygen minimum zone studied using a mesoscale eddy as a natural tracer experiment. Global Biogeochemical Cycles 29, 793–811.
| N-loss isotope effects in the Peru oxygen minimum zone studied using a mesoscale eddy as a natural tracer experiment.Crossref | GoogleScholarGoogle Scholar |
Braker, G., Zhou, J., Wu, L., Devol, A. H., and Tiedje, J. M. (2000). Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Applied and Environmental Microbiology 66, 2096–2104.
| Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities.Crossref | GoogleScholarGoogle Scholar | 10788387PubMed |
Brin, L. D., Giblin, A. E., and Rich, J. J. (2014). Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnology and Oceanography 59, 851–860.
| Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments.Crossref | GoogleScholarGoogle Scholar |
Caffrey, J. M., Bano, N., Kalanetra, K., and Hollibaugh, J. T. (2007). Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. The ISME Journal 1, 660–662.
| Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia.Crossref | GoogleScholarGoogle Scholar | 18043673PubMed |
Casciotti, K. L., Forbes, M., Vedamati, J., Peters, B., Martin, T., and Mordy, C. W. (2018). Nitrous oxide cycling in the Eastern Tropical South Pacific as inferred from isotopic and isotopomeric data. Deep-sea Research. Part II, Topical Studies in Oceanography 156, 155–167.
| Nitrous oxide cycling in the Eastern Tropical South Pacific as inferred from isotopic and isotopomeric data.Crossref | GoogleScholarGoogle Scholar |
Castro-Gonzalez, M., Braker, G., Farias, L., and Ulloa, O. (2005). Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific. Environmental Microbiology 7, 1298–1306.
| Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific.Crossref | GoogleScholarGoogle Scholar | 16104853PubMed |
Codispoti, L. A., Brandes, J. A., Christensen, J. P., Devol, A. H., Naqvi, S. W. A., Paerl, H. W., and Yoshinari, T. (2001). The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Scientia Marina 65, 85–105.
| The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene?Crossref | GoogleScholarGoogle Scholar |
Coria-Monter, E., Monreal-Gómez, M. A., Salas-de-León, D. A., Aldeco-Ramírez, J., and Merino-Ibarra, M. (2014). Differential distribution of diatoms and dinoflagellates in a cyclonic eddy confined in the Bay of La Paz, Gulf of California. Journal of Geophysical Research. Oceans 119, 6258–6268.
| Differential distribution of diatoms and dinoflagellates in a cyclonic eddy confined in the Bay of La Paz, Gulf of California.Crossref | GoogleScholarGoogle Scholar |
Coria-Monter, E., Monreal-Gómez, M. A., Salas de León, D. A., Durán-Campos, E., and Merino-Ibarra, M. (2017). Wind driven nutrient and subsurface chlorophyll-a enhancement in the Bay of La Paz, Gulf of California. Estuarine, Coastal and Shelf Science 196, 290–300.
| Wind driven nutrient and subsurface chlorophyll-a enhancement in the Bay of La Paz, Gulf of California.Crossref | GoogleScholarGoogle Scholar |
Dalsgaard, T., Thamdrup, B., Farías, L., and Revsbech, N. P. (2012). Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnology and Oceanography 57, 1331–1346.
| Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific.Crossref | GoogleScholarGoogle Scholar |
Dalsgaard, T., Stewart, F. J., Thamdrup, B., De Brabandere, L., Revsbech, N. P., Ulloa, O., Canfield, D. E., and DeLong, E. F. (2014). Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off northern Chile. mBio 5, e01966-14–4.
| Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off northern Chile.Crossref | GoogleScholarGoogle Scholar | 25352619PubMed |
Deutsch, C., Gruber, N., Key, R. M., Sarmiento, J. L., and Ganachaud, A. (2001). Denitrification and N2 fixation in the Pacific Ocean. Global Biogeochemical Cycles 15, 483–506.
| Denitrification and N2 fixation in the Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Duran-Campos, E., Salas-de-León, D. A., Monreal-Gómez, M. A., Aldeco-Ramírez, J., and Coria-Monter, E. (2015). Differential zooplankton aggregation due to relative vorticity in a semi-enclosed bay. Estuarine, Coastal and Shelf Science 164, 10–18.
| Differential zooplankton aggregation due to relative vorticity in a semi-enclosed bay.Crossref | GoogleScholarGoogle Scholar |
Ewart, C. S., Meyers, M. K., Wallner, E. R., McGillicuddy, D. J., and Carlson, C. A. (2008). Microbial dynamics in cyclonic and anticyclonic mode-water eddies in the northwestern Sargasso Sea. Deep-sea Research. Part II, Topical Studies in Oceanography 55, 1334–1347.
| Microbial dynamics in cyclonic and anticyclonic mode-water eddies in the northwestern Sargasso Sea.Crossref | GoogleScholarGoogle Scholar |
Falkowski, P. G. (1997). Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275.
| Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean.Crossref | GoogleScholarGoogle Scholar |
Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., and Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America 102, 14683–14688.
| Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Crossref | GoogleScholarGoogle Scholar | 16186488PubMed |
Glibert, P. M., Wilkerson, F. P., Dugdale, R. C., Raven, J. A., Dupont, C. L., Leavitt, P. R., Parker, A. E., Burkholder, J. M., and Kana, T. M. (2016). Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnology and Oceanography 61, 165–197.
| Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions.Crossref | GoogleScholarGoogle Scholar |
Graf, D. R. H., Jones, C. M., and Hallin, S. (2014). Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS One 9, e114118.
| Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions.Crossref | GoogleScholarGoogle Scholar |
Graham, M. H. (2003). Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815.
| Confronting multicollinearity in ecological multiple regression.Crossref | GoogleScholarGoogle Scholar |
Gruber, N., and Sarmiento, J. L. (1997). Global patterns of marine nitrogen fixation and denitrification. Global Biogeochemical Cycles 11, 235–266.
| Global patterns of marine nitrogen fixation and denitrification.Crossref | GoogleScholarGoogle Scholar |
Grundle, D. S., Löscher, C. R., Krahmann, G., Altabet, M. A., Bange, H. W., Karstensen, J., Körtzinger, A., and Fiedler, B. (2017). Low oxygen eddies in the eastern tropical North Atlantic: implications for N2O cycling. Scientific Reports 7, 4806.
| Low oxygen eddies in the eastern tropical North Atlantic: implications for N2O cycling.Crossref | GoogleScholarGoogle Scholar | 28684772PubMed |
Hansen, H. P., and Koroleff, F. (1999). Determination of nutrients. In ‘Methods of Seawater Analysis’. (Eds K. Grasshoff, K. Kremling, and M. Ehrhardt.) pp. 159–228. (Wiley-VCH Verlag GmbH: Weinheim, Germany.)
Henry, S., Baudoin, E., López-Gutiérrez, J. C., Martin-Laurent, F., Brauman, A., and Philippot, L. (2004). Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods 59, 327–335.
| Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR.Crossref | GoogleScholarGoogle Scholar | 15488276PubMed |
Hofmann, A. F., Peltzer, E. T., Walz, P. M., and Brewer, P. G. (2011). Hypoxia by degrees: establishing definitions for a changing ocean. Deep-sea Research. Part I, Oceanographic Research Papers 58, 1212–1226.
| Hypoxia by degrees: establishing definitions for a changing ocean.Crossref | GoogleScholarGoogle Scholar |
Horak, R. E. A., Ruef, W., Ward, B. B., and Devol, A. H. (2016). Expansion of denitrification and anoxia in the eastern tropical North Pacific from 1972 to 2012. Geophysical Research Letters 43, 5252–5260.
| Expansion of denitrification and anoxia in the eastern tropical North Pacific from 1972 to 2012.Crossref | GoogleScholarGoogle Scholar |
IOC, SCOR and IAPSO (2010). ‘The International Thermodynamic Equation of Seawater 2010. Calculation and use of Thermodynamic Properties. Manuals and Guides No. 56.’ (Intergovernmental Oceanographic Commission, UNESCO.)
IPCC (2013). ‘Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Eds T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley.) (Cambridge University Press: Cambridge, UK.)
Jayakumar, D., Francis, C. A., Naqvi, S. W. A., and Ward, B. B. (2004). Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea. Aquatic Microbial Ecology 34, 69–78.
| Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea.Crossref | GoogleScholarGoogle Scholar |
Jayakumar, A., Peng, X., and Ward, B. (2013). Community composition of bacteria involved in fixed nitrogen loss in the water column of two major oxygen minimum zones in the ocean. Aquatic Microbial Ecology 70, 245–259.
| Community composition of bacteria involved in fixed nitrogen loss in the water column of two major oxygen minimum zones in the ocean.Crossref | GoogleScholarGoogle Scholar |
Ka, J. O., Urbance, J., Ye, R. W., Ahn, T. Y., and Tiedje, J. M. (1997). Diversity of oxygen and N-oxide regulation of nitrite reductases in denitrifying bacteria. FEMS Microbiology Letters 156, 55–60.
| Diversity of oxygen and N-oxide regulation of nitrite reductases in denitrifying bacteria.Crossref | GoogleScholarGoogle Scholar | 9368361PubMed |
Kalvelage, T., Jensen, M. M., Contreras, S., Revsbech, N. P., Lam, P., Günter, M., LaRoche, J., Lavik, G., and Kuypers, M. M. M. (2011). Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS One 6, e29299.
| Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones.Crossref | GoogleScholarGoogle Scholar | 22216239PubMed |
Kalvelage, T., Lavik, G., Lam, P., Contreras, S., Arteaga, L., Loscher, C. R., Oschlies, A., Paulmier, A., Stramma, L., Kuypers, M. M. M., Löscher, C. R., Oschlies, A., Paulmier, A., Stramma, L., and Kuypers, M. M. M. (2013). Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nature Geoscience 6, 228–234.
| Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone.Crossref | GoogleScholarGoogle Scholar |
Kartal, B., Kuypers, M. M. M. M., Lavik, G., Schalk, J., Op Den Camp, H. J. M. M., Jetten, M. S. M. M., and Strous, M. (2007). Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environmental Microbiology 9, 635–642.
| Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium.Crossref | GoogleScholarGoogle Scholar | 17298364PubMed |
Klein, P., and Lapeyre, G. (2009). The oceanic vertical pump induced by mesoscale and submesoscale turbulence. Annual Review of Marine Science 1, 351–375.
| The oceanic vertical pump induced by mesoscale and submesoscale turbulence.Crossref | GoogleScholarGoogle Scholar | 21141041PubMed |
Kock, A., Arevalo-Martinez, D. L., Loscher, C. R., and Bange, H. W. (2016). Extreme N2O accumulation in the coastal oxygen minimum zone off Peru. Biogeosciences 13, 827–840.
| Extreme N2O accumulation in the coastal oxygen minimum zone off Peru.Crossref | GoogleScholarGoogle Scholar |
Kong, L., Jing, H., Kataoka, T., Buchwald, C., and Liu, H. (2013). Diversity and spatial distribution of hydrazine oxidoreductase (hzo) gene in the oxygen minimum zone off Costa Rica. PLoS One 8, e78275.
| Diversity and spatial distribution of hydrazine oxidoreductase (hzo) gene in the oxygen minimum zone off Costa Rica.Crossref | GoogleScholarGoogle Scholar | 24386201PubMed |
Lam, P., Lavik, G., Jensen, M. M., van de Vossenberg, J., Schmid, M., Woebken, D., Gutierrez, D., Amann, R., Jetten, M. S. M., and Kuypers, M. M. M. (2009). Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proceedings of the National Academy of Sciences of the United States of America 106, 4752–4757.
| Revising the nitrogen cycle in the Peruvian oxygen minimum zone.Crossref | GoogleScholarGoogle Scholar | 19255441PubMed |
Lavín, M. F., Castro, R., Beier, E., Godínez, V. M., Amador, A., and Guest, P. (2009). SST, thermohaline structure, and circulation in the southern Gulf of California in June 2004 during the North American Monsoon Experiment. Journal of Geophysical Research 114, C02025.
| SST, thermohaline structure, and circulation in the southern Gulf of California in June 2004 during the North American Monsoon Experiment.Crossref | GoogleScholarGoogle Scholar |
Lee, J. A., and Francis, C. A. (2017). Spatiotemporal characterization of San Francisco bay denitrifying communities: a comparison of nirK and nirS diversity and abundance. Microbial Ecology 73, 271–284.
| Spatiotemporal characterization of San Francisco bay denitrifying communities: a comparison of nirK and nirS diversity and abundance.Crossref | GoogleScholarGoogle Scholar | 27709247PubMed |
Li, M., Hong, Y., Klotz, M. G., and Gu, J. D. (2010). A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Applied Microbiology and Biotechnology 86, 781–790.
| A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments.Crossref | GoogleScholarGoogle Scholar | 20107988PubMed |
Löscher, C. R., Fischer, M. A., Neulinger, S. C., Fiedler, B., Philippi, M., Schütte, F., Singh, A., Hauss, H., Karstensen, J., Körtzinger, A., Künzel, S., and Schmitz, R. A. (2015). Hidden biosphere in an oxygen-deficient Atlantic open-ocean eddy: future implications of ocean deoxygenation on primary production in the eastern tropical North Atlantic. Biogeosciences 12, 7467–7482.
| Hidden biosphere in an oxygen-deficient Atlantic open-ocean eddy: future implications of ocean deoxygenation on primary production in the eastern tropical North Atlantic.Crossref | GoogleScholarGoogle Scholar |
Löscher, C. R., Mohr, W., Bange, H. W., and Canfield, D. E. (2020). No nitrogen fixation in the Bay of Bengal? Biogeosciences 17, 851–864.
| No nitrogen fixation in the Bay of Bengal?Crossref | GoogleScholarGoogle Scholar |
McGillicuddy, D. J., Robinson, A. R., Siegel, D. A., Jannasch, H. W., Johnson, R., Dickey, T. D., McNeil, J., Michaels, A. F., and Knap, A. H. (1998). Influence of mesoscale eddies on new production in the Sargasso Sea. Nature 394, 263–266.
| Influence of mesoscale eddies on new production in the Sargasso Sea.Crossref | GoogleScholarGoogle Scholar |
McGillicuddy, D. J., Anderson, L. A., Bates, N. R., Bibby, T., Buesseler, K. O., Carlson, C. A., Davis, C. S., Ewart, C., Falkowski, P. G., Goldthwait, S. A., Hansell, D. A., Jenkins, W. J., Johnson, R., Kosnyrev, V. K., Ledwell, J. R., Li, Q. P., Siegel, D. A., and Steinberg, D. K. (2007). Eddy/wind interactions stimulate extraordinary mid-ocean plankton blooms. Science 316, 1021–1026.
| Eddy/wind interactions stimulate extraordinary mid-ocean plankton blooms.Crossref | GoogleScholarGoogle Scholar | 17510363PubMed |
Michotey, V., Méjean, V., and Bonin, P. (2000). Comparison of methods for quantification of cytochrome cd1-denitrifying bacteria in environmental marine samples. Applied and Environmental Microbiology 66, 1564–1571.
| Comparison of methods for quantification of cytochrome cd1-denitrifying bacteria in environmental marine samples.Crossref | GoogleScholarGoogle Scholar | 10742243PubMed |
Mincer, T. J., Church, M. J., Taylor, L. T., Preston, C., Karl, D. M., and DeLong, E. F. (2007). Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environmental Microbiology 9, 1162–1175.
| Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre.Crossref | GoogleScholarGoogle Scholar | 17472632PubMed |
Mohan, S. B., Schmid, M., Jetten, M., and Cole, J. (2004). Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiology Ecology 49, 433–443.
| Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification.Crossref | GoogleScholarGoogle Scholar | 19712292PubMed |
Monreal-Gómez, M. A., Molina-Cruz, A., and Salas-de-León, D. A. (2001). Water masses and cyclonic circulation in Bay of La Paz, Gulf of California, during June 1998. Journal of Marine Systems 30, 305–315.
| Water masses and cyclonic circulation in Bay of La Paz, Gulf of California, during June 1998.Crossref | GoogleScholarGoogle Scholar |
Newell, S. E., Babbin, A. R., Jayakumar, D., Ward, B. B., Jayakumar, A., and Ward, B. B. (2011). Ammonia oxidation rates and nitrification in the Arabian Sea. Global Biogeochemical Cycles 25, GB4016.
| Ammonia oxidation rates and nitrification in the Arabian Sea.Crossref | GoogleScholarGoogle Scholar |
Newell, S. E., Fawcett, S. E., and Ward, B. B. (2013). Depth distribution of ammonia oxidation rates and ammonia-oxidizer community composition in the Sargasso Sea. Limnology and Oceanography 58, 1491–1500.
| Depth distribution of ammonia oxidation rates and ammonia-oxidizer community composition in the Sargasso Sea.Crossref | GoogleScholarGoogle Scholar |
Pajares, S., and Ramos, R. (2019). Processes and microorganisms involved in the marine nitrogen cycle: knowledge and gaps. Frontiers in Marine Science 6, 739.
| Processes and microorganisms involved in the marine nitrogen cycle: knowledge and gaps.Crossref | GoogleScholarGoogle Scholar |
Pajares, S., Soto-Jiménez, M. F., and Merino-Ibarra, M. (2019). Molecular and isotopic evidence of the distribution of nitrogen-cycling microbial communities in the oxygen minimum zone of the Tropical Mexican Pacific. FEMS Microbiology Ecology 95, fiz143.
| Molecular and isotopic evidence of the distribution of nitrogen-cycling microbial communities in the oxygen minimum zone of the Tropical Mexican Pacific.Crossref | GoogleScholarGoogle Scholar | 31557275PubMed |
Paulmier, A., and Ruiz-Pino, D. (2009). Oxygen minimum zones (OMZs) in the modern ocean. Progress in Oceanography 80, 113–128.
| Oxygen minimum zones (OMZs) in the modern ocean.Crossref | GoogleScholarGoogle Scholar |
Peng, X., Fuchsman, C. A., Jayakumar, A., Warner, M. J., Devol, A. H., and Ward, B. B. (2016). Revisiting nitrification in the Eastern Tropical South Pacific: a focus on controls. Journal of Geophysical Research. Oceans 121, 1667–1684.
| Revisiting nitrification in the Eastern Tropical South Pacific: a focus on controls.Crossref | GoogleScholarGoogle Scholar |
Philips, S., and Verstraete, W. (2001). Effect of repeated addition of nitrite to semi-continuous activated sludge reactors. Bioresource Technology 80, 73–82.
| Effect of repeated addition of nitrite to semi-continuous activated sludge reactors.Crossref | GoogleScholarGoogle Scholar | 11554604PubMed |
Piper, D. Z. (1991). Geochemistry of Tertiary sedimentary phosphate deposit: Baja California Sur, México. Chemical Geology 92, 283–316.
| Geochemistry of Tertiary sedimentary phosphate deposit: Baja California Sur, México.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2016). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.Rproject.org.
Ravishankara, A. R., Daniel, J. S., and Portmann, R. W. (2009). Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125.
| Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century.Crossref | GoogleScholarGoogle Scholar | 19713491PubMed |
Rotthauwe, J. H., Witzel, K. P., and Liesack, W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology 63, 4704–4712.
| The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations.Crossref | GoogleScholarGoogle Scholar | 9406389PubMed |
Sánchez-Velasco, L., Beier, E., Ávalos-García, C., and Lavín, M. F. (2006). Larval fish assemblages and geostrophic circulation in Bahía de la Paz and the surrounding region of the Gulf of California. Journal of Plankton Research 28, 1081–1098.
| Larval fish assemblages and geostrophic circulation in Bahía de la Paz and the surrounding region of the Gulf of California.Crossref | GoogleScholarGoogle Scholar |
Santoro, A. E., Casciotti, K. L., and Francis, C. A. (2010). Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environmental Microbiology 12, 1989–2006.
| Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current.Crossref | GoogleScholarGoogle Scholar | 20345944PubMed |
Schlitzer, R. (2015). Data analysis and visualization with Ocean Data View. CMOS Bulletin SCMO 43, 9–13.
Schütte, F., Karstensen, J., Krahmann, G., Hauss, H., Fiedler, B., Brandt, P., Visbeck, M., and Körtzinger, A. (2016). Characterization of ‘dead-zone’ eddies in the eastern tropical North Atlantic. Biogeosciences 13, 5865–5881.
| Characterization of ‘dead-zone’ eddies in the eastern tropical North Atlantic.Crossref | GoogleScholarGoogle Scholar |
Song, B., Lisa, J. A., and Tobias, C. R. (2014). Linking DNRA community structure and activity in a shallow lagoonal estuarine system. Frontiers in Microbiology 5, 460.
| Linking DNRA community structure and activity in a shallow lagoonal estuarine system.Crossref | GoogleScholarGoogle Scholar | 25232351PubMed |
Stramma, L., Bange, H. W., Czeschel, R., Lorenzo, A., and Frank, M. (2013). On the role of mesoscale eddies for the biological productivity and biogeochemistry in the eastern tropical Pacific Ocean off Peru. Biogeosciences 10, 7293–7306.
| On the role of mesoscale eddies for the biological productivity and biogeochemistry in the eastern tropical Pacific Ocean off Peru.Crossref | GoogleScholarGoogle Scholar |
Venkatachalam, S., Ansorge, I. J., Mendes, A., Melato, L. I., Matcher, G. F., and Dorrington, R. A. (2017). A pivotal role for ocean eddies in the distribution of microbial communities across the Antarctic Circumpolar Current. PLoS One 12, e0183400.
| A pivotal role for ocean eddies in the distribution of microbial communities across the Antarctic Circumpolar Current.Crossref | GoogleScholarGoogle Scholar | 28827834PubMed |
Ward, B. B. B., Devol, A. H., Rich, J. J., Chang, B. X., Bulow, S. E., Naik, H., Pratihary, A., Jayakumar, A., and Jayakumar, D. (2009). Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461, 78–81.
| Denitrification as the dominant nitrogen loss process in the Arabian Sea.Crossref | GoogleScholarGoogle Scholar |
Welsh, A., Chee-Sanford, J. C., Connor, L. M., Löffler, F. E., and Sanford, R. A. (2014). Refined NrfA phylogeny improves PCR-based nrfA gene detection. Applied and Environmental Microbiology 80, 2110–2119.
| Refined NrfA phylogeny improves PCR-based nrfA gene detection.Crossref | GoogleScholarGoogle Scholar | 24463965PubMed |
Zuur, A. F., Ieno, E. N., and Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.
| A protocol for data exploration to avoid common statistical problems.Crossref | GoogleScholarGoogle Scholar |
