Articles | Volume 19, issue 11
https://doi.org/10.5194/bg-19-2939-2022
© Author(s) 2022. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-19-2939-2022
© Author(s) 2022. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Controlling factors on the global distribution of a representative marine non-cyanobacterial diazotroph phylotype (Gamma A)
Zhibo Shao
State Key Laboratory of Marine Environmental Science, College of
Ocean and Earth Sciences, Xiamen University, Xiamen, Fujian 361102, China
State Key Laboratory of Marine Environmental Science, College of
Ocean and Earth Sciences, Xiamen University, Xiamen, Fujian 361102, China
Related authors
Zhibo Shao, Yangchun Xu, Hua Wang, Weicheng Luo, Lice Wang, Yuhong Huang, Nona Sheila R. Agawin, Ayaz Ahmed, Mar Benavides, Mikkel Bentzon-Tilia, Ilana Berman-Frank, Hugo Berthelot, Isabelle C. Biegala, Mariana B. Bif, Antonio Bode, Sophie Bonnet, Deborah A. Bronk, Mark V. Brown, Lisa Campbell, Douglas G. Capone, Edward J. Carpenter, Nicolas Cassar, Bonnie X. Chang, Dreux Chappell, Yuh-ling Lee Chen, Matthew J. Church, Francisco M. Cornejo-Castillo, Amália Maria Sacilotto Detoni, Scott C. Doney, Cecile Dupouy, Marta Estrada, Camila Fernandez, Bieito Fernández-Castro, Debany Fonseca-Batista, Rachel A. Foster, Ken Furuya, Nicole Garcia, Kanji Goto, Jesús Gago, Mary R. Gradoville, M. Robert Hamersley, Britt A. Henke, Cora Hörstmann, Amal Jayakumar, Zhibing Jiang, Shuh-Ji Kao, David M. Karl, Leila R. Kittu, Angela N. Knapp, Sanjeev Kumar, Julie LaRoche, Hongbin Liu, Jiaxing Liu, Caroline Lory, Carolin R. Löscher, Emilio Marañón, Lauren F. Messer, Matthew M. Mills, Wiebke Mohr, Pia H. Moisander, Claire Mahaffey, Robert Moore, Beatriz Mouriño-Carballido, Margaret R. Mulholland, Shin-ichiro Nakaoka, Joseph A. Needoba, Eric J. Raes, Eyal Rahav, Teodoro Ramírez-Cárdenas, Christian Furbo Reeder, Lasse Riemann, Virginie Riou, Julie C. Robidart, Vedula V. S. S. Sarma, Takuya Sato, Himanshu Saxena, Corday Selden, Justin R. Seymour, Dalin Shi, Takuhei Shiozaki, Arvind Singh, Rachel E. Sipler, Jun Sun, Koji Suzuki, Kazutaka Takahashi, Yehui Tan, Weiyi Tang, Jean-Éric Tremblay, Kendra Turk-Kubo, Zuozhu Wen, Angelicque E. White, Samuel T. Wilson, Takashi Yoshida, Jonathan P. Zehr, Run Zhang, Yao Zhang, and Ya-Wei Luo
Earth Syst. Sci. Data, 15, 3673–3709, https://doi.org/10.5194/essd-15-3673-2023, https://doi.org/10.5194/essd-15-3673-2023, 2023
Short summary
Short summary
N2 fixation by marine diazotrophs is an important bioavailable N source to the global ocean. This updated global oceanic diazotroph database increases the number of in situ measurements of N2 fixation rates, diazotrophic cell abundances, and nifH gene copy abundances by 184 %, 86 %, and 809 %, respectively. Using the updated database, the global marine N2 fixation rate is estimated at 223 ± 30 Tg N yr−1, which triplicates that using the original database.
Zhibo Shao, Yangchun Xu, Hua Wang, Weicheng Luo, Lice Wang, Yuhong Huang, Nona Sheila R. Agawin, Ayaz Ahmed, Mar Benavides, Mikkel Bentzon-Tilia, Ilana Berman-Frank, Hugo Berthelot, Isabelle C. Biegala, Mariana B. Bif, Antonio Bode, Sophie Bonnet, Deborah A. Bronk, Mark V. Brown, Lisa Campbell, Douglas G. Capone, Edward J. Carpenter, Nicolas Cassar, Bonnie X. Chang, Dreux Chappell, Yuh-ling Lee Chen, Matthew J. Church, Francisco M. Cornejo-Castillo, Amália Maria Sacilotto Detoni, Scott C. Doney, Cecile Dupouy, Marta Estrada, Camila Fernandez, Bieito Fernández-Castro, Debany Fonseca-Batista, Rachel A. Foster, Ken Furuya, Nicole Garcia, Kanji Goto, Jesús Gago, Mary R. Gradoville, M. Robert Hamersley, Britt A. Henke, Cora Hörstmann, Amal Jayakumar, Zhibing Jiang, Shuh-Ji Kao, David M. Karl, Leila R. Kittu, Angela N. Knapp, Sanjeev Kumar, Julie LaRoche, Hongbin Liu, Jiaxing Liu, Caroline Lory, Carolin R. Löscher, Emilio Marañón, Lauren F. Messer, Matthew M. Mills, Wiebke Mohr, Pia H. Moisander, Claire Mahaffey, Robert Moore, Beatriz Mouriño-Carballido, Margaret R. Mulholland, Shin-ichiro Nakaoka, Joseph A. Needoba, Eric J. Raes, Eyal Rahav, Teodoro Ramírez-Cárdenas, Christian Furbo Reeder, Lasse Riemann, Virginie Riou, Julie C. Robidart, Vedula V. S. S. Sarma, Takuya Sato, Himanshu Saxena, Corday Selden, Justin R. Seymour, Dalin Shi, Takuhei Shiozaki, Arvind Singh, Rachel E. Sipler, Jun Sun, Koji Suzuki, Kazutaka Takahashi, Yehui Tan, Weiyi Tang, Jean-Éric Tremblay, Kendra Turk-Kubo, Zuozhu Wen, Angelicque E. White, Samuel T. Wilson, Takashi Yoshida, Jonathan P. Zehr, Run Zhang, Yao Zhang, and Ya-Wei Luo
Earth Syst. Sci. Data, 15, 3673–3709, https://doi.org/10.5194/essd-15-3673-2023, https://doi.org/10.5194/essd-15-3673-2023, 2023
Short summary
Short summary
N2 fixation by marine diazotrophs is an important bioavailable N source to the global ocean. This updated global oceanic diazotroph database increases the number of in situ measurements of N2 fixation rates, diazotrophic cell abundances, and nifH gene copy abundances by 184 %, 86 %, and 809 %, respectively. Using the updated database, the global marine N2 fixation rate is estimated at 223 ± 30 Tg N yr−1, which triplicates that using the original database.
Hyewon Heather Kim, Jeff S. Bowman, Ya-Wei Luo, Hugh W. Ducklow, Oscar M. Schofield, Deborah K. Steinberg, and Scott C. Doney
Biogeosciences, 19, 117–136, https://doi.org/10.5194/bg-19-117-2022, https://doi.org/10.5194/bg-19-117-2022, 2022
Short summary
Short summary
Heterotrophic marine bacteria are tiny organisms responsible for taking up organic matter in the ocean. Using a modeling approach, this study shows that characteristics (taxonomy and physiology) of bacteria are associated with a subset of ecological processes in the coastal West Antarctic Peninsula region, a system susceptible to global climate change. This study also suggests that bacteria will become more active, in particular large-sized cells, in response to changing climates in the region.
Hyewon Heather Kim, Ya-Wei Luo, Hugh W. Ducklow, Oscar M. Schofield, Deborah K. Steinberg, and Scott C. Doney
Geosci. Model Dev., 14, 4939–4975, https://doi.org/10.5194/gmd-14-4939-2021, https://doi.org/10.5194/gmd-14-4939-2021, 2021
Short summary
Short summary
The West Antarctic Peninsula (WAP) is a rapidly warming region, revealed by multi-decadal observations. Despite the region being data rich, there is a lack of focus on ecosystem model development. Here, we introduce a data assimilation ecosystem model for the WAP region. Experiments by assimilating data from an example growth season capture key WAP features. This study enables us to glue the snapshots from available data sets together to explain the observations in the WAP.
Le Xie, Wei Wei, Lanlan Cai, Xiaowei Chen, Yuhong Huang, Nianzhi Jiao, Rui Zhang, and Ya-Wei Luo
Earth Syst. Sci. Data, 13, 1251–1271, https://doi.org/10.5194/essd-13-1251-2021, https://doi.org/10.5194/essd-13-1251-2021, 2021
Short summary
Short summary
Viruses play key roles in marine ecosystems by killing their hosts, maintaining diversity and recycling nutrients. In the global viral oceanography database (gVOD), 10 931 viral abundance data and 727 viral production data, along with host and other oceanographic parameters, were compiled. It identified viral data were undersampled in the southeast Pacific and Indian oceans. The gVOD can be used in marine viral ecology investigation and modeling of marine ecosystems and biogeochemical cycles.
Cited articles
Abraham, E. R.: The generation of plankton patchiness by turbulent
stirring, Nature, 391, 577–580, https://doi.org/10.1038/35361,
1998.
Behrenfeld, M. J. and Falkowski, P. G.: A consumer's guide to phytoplankton
primary productivity models, Limnol. Oceanogr., 42, 1479–1491, https://doi.org/10.4319/lo.1997.42.7.1479, 1997.
Benavides, M. and Robidart, J.: Bridging the spatiotemporal gap in
diazotroph activity and diversity with high-resolution measurements, Front.
Mar. Sci., 7, 568876, https://doi.org/10.3389/fmars.2020.568876, 2020.
Benavides, M., Moisander, P. H., Daley, M. C., Bode, A., and Aristegui, J.:
Longitudinal variability of diazotroph abundances in the subtropical North
Atlantic Ocean, J. Plankton Res., 38, 662–672, https://doi.org/10.1093/plankt/fbv121, 2016.
Benavides, M., Bonnet, S., Berman-Frank, I., and Riemann, L.: Deep into
oceanic N2 fixation, Front. Mar. Sci., 5, 108, https://doi.org/10.3389/fmars.2018.00108, 2018.
Bentzon-Tilia, M., Severin, I., Hansen, L. H., and Riemann, L.: Genomics and
ecophysiology of heterotrophic nitrogen-fixing bacteria isolated from
estuarine surface water, mBio, 6, e00929-15, https://doi.org/10.1128/mBio.00929-15, 2015.
Berthelot, H., Benavides, M., Moisander, P. H., Grosso, O., and Bonnet, S.:
High-nitrogen fixation rates in the particulate and dissolved pools in the
Western Tropical Pacific (Solomon and Bismarck Seas), Geophys. Res. Lett.,
44, 8414–8423, https://doi.org/10.1002/2017gl073856, 2017.
Bird, C. and Wyman, M.: Transcriptionally active heterotrophic diazotrophs
are widespread in the upper water column of the Arabian Sea, FEMS
Microbiol. Ecol., 84, 189–200, https://doi.org/10.1111/1574-6941.12049, 2013.
Bird, C., Martinez, M. J., O'Donnell, A. G., and Wyman, M.: Spatial
distribution and transcriptional activity of an uncultured clade of
planktonic diazotrophic γ-proteobacteria in the Arabian Sea, Appl. Environ. Microbiol., 71, 2079–2085, https://doi.org/10.1128/AEM.71.4.2079-2085.2005, 2005.
Bombar, D., Moisander, P. H., Dippner, J. W., Foster, R. A., Voss, M.,
Karfeld, B., and Zehr, J. P.: Distribution of diazotrophic microorganisms
and nifH gene expression in the Mekong River plume during intermonsoon, Mar.
Ecol.-Prog. Ser., 424, 39–55, https://doi.org/10.3354/meps08976, 2011.
Bombar, D., Paerl, R. W., and Riemann, L.: Marine non-cyanobacterial
diazotrophs: moving beyond molecular detection, Trends Microbiol., 24,
916–927, https://doi.org/10.1016/j.tim.2016.07.002, 2016.
Bonnet, S., Guieu, C., Bruyant, F., Prášil, O., Van Wambeke, F., Raimbault, P., Moutin, T., Grob, C., Gorbunov, M. Y., Zehr, J. P., Masquelier, S. M., Garczarek, L., and Claustre, H.: Nutrient limitation of primary productivity in the Southeast Pacific (BIOSOPE cruise), Biogeosciences, 5, 215–225, https://doi.org/10.5194/bg-5-215-2008, 2008.
Bonnet, S., Dekaezemacker, J., Turk-Kubo, K. A., Moutin, T., Hamersley, R.
M., Grosso, O., Zehr, J. P., and Capone, D. G.: Aphotic N2 fixation in
the Eastern Tropical South Pacific Ocean, PLoS One, 8, e81265, https://doi.org/10.1371/journal.pone.0081265, 2013.
Boyd, P. W. and Ellwood, M. J.: The biogeochemical cycle of iron in the
ocean, Nat. Geosci., 3, 675–682, https://doi.org/10.1038/ngeo964,
2010.
Boyer, T. P., Garcia, H. E., Locarnini, R. A., Zweng, M. M., Mishonov, A. V., Reagan, J. R., Weathers, K. A., Baranova, O. K., Seidov, D., and Smolyar, I. V.: World Ocean Atlas 2018, NOAA [dataset], https://www.ncei.noaa.gov/archive/accession/NCEI-WOA18, last access: 11 June 2022.
Chelton, D. B., Schlax, M. G., and Samelson, R. M.: Global observations of
nonlinear mesoscale eddies, Prog. Oceanogr., 91, 167–216, https://doi.org/10.1016/j.pocean.2011.01.002, 2011.
Chen, M. M., Lu, Y. Y., Jiao, N. Z., Tian, J. W., Kao, S. J., and Zhang, Y.:
Biogeographic drivers of diazotrophs in the western Pacific Ocean, Limnol.
Oceanogr., 64, 1403–1421, https://doi.org/10.1002/lno.11123,
2019.
Chen, T. Y., Chen, Y. L. L., Sheu, D. S., Chen, H. Y., Lin, Y. H., and
Shiozaki, T.: Community and abundance of heterotrophic diazotrophs in the
northern South China Sea: Revealing the potential importance of a new
alphaproteobacterium in N2 fixation, Deep-Sea Res. Pt. I, 143, 104–114,
https://doi.org/10.1016/j.dsr.2018.11.006, 2019.
Cheung, S., Zehr, J. P., Xia, X., Tsurumoto, C., Endo, H., Nakaoka, S.-i.,
Mak, W., Suzuki, K., and Liu, H.: Gamma4: a genetically versatile
Gammaproteobacterial nifH phylotype that is widely distributed in the North
Pacific Ocean, Environ. Microbiol., 23, 4246–4259, https://doi.org/10.1111/1462-2920.15604, 2021.
Cheung, S. Y., Nitanai, R., Tsurumoto, C., Endo, H., Nakaoka, S., Cheah, W.,
Lorda, J. F., Xia, X. M., Liu, H. B., and Suzuki, K.: Physical forcing
controls the basin-scale occurrence of nitrogen-fixing organisms in the
North Pacific Ocean, Global Biogeochem. Cy., 34, e2019GB006452, https://doi.org/10.1029/2019GB006452, 2020.
Church, M. J., Mahaffey, C., Letelier, R. M., Lukas, R., Zehr, J. P., and
Karl, D. M.: Physical forcing of nitrogen fixation and diazotroph community
structure in the North Pacific subtropical gyre, Global Biogeochem. Cy., 23,
GB2020, https://doi.org/10.1029/2008gb003418, 2009.
Crameri, F., Shephard, G. E., and Heron, P. J.: The misuse of colour in
science communication, Nat. Commun., 11, 5444, https://doi.org/10.1038/s41467-020-19160-7, 2020.
Davis, C. S. and McGillicuddy Jr., D. J.: Transatlantic abundance of the
N2-fixing colonial cyanobacterium Trichodesmium, Science, 312, 1517–1520, https://doi.org/10.1126/science.1123570, 2006.
de Boyer Montégut, C., Madec, G., Fischer, A. S., Lazar, A., and
Iudicone, D.: Mixed layer depth over the global ocean: An examination of
profile data and a profile-based climatology, J. Geophys. Res.-Oceans, 109,
C12003, https://doi.org/10.1029/2004JC002378, 2004.
Dekaezemacker, J., Bonnet, S., Grosso, O., Moutin, T., Bressac, M., and
Capone, D. G.: Evidence of active dinitrogen fixation in surface waters of
the eastern tropical South Pacific during El Nino and La Nina events and
evaluation of its potential nutrient controls, Global Biogeochem. Cy., 27,
768–779, https://doi.org/10.1002/gbc.20063, 2013.
Delmont, T. O., Quince, C., Shaiber, A., Esen, O. C., Lee, S. T. M., Rappe,
M. S., MacLellan, S. L., Lucker, S., and Eren, A. M.: Nitrogen-fixing
populations of Planctomycetes and Proteobacteria are abundant in surface
ocean metagenomes, Nat. Microbiol, 3, 804–813, https://doi.org/10.1038/s41564-018-0176-9, 2018.
Delmont, T. O., Pierella Karlusich, J. J., Veseli, I., Fuessel, J., Eren, A.
M., Foster, R. A., Bowler, C., Wincker, P., and Pelletier, E.: Heterotrophic
bacterial diazotrophs are more abundant than their cyanobacterial
counterparts in metagenomes covering most of the sunlit ocean, ISME
J., 16, 927–936, https://doi.org/10.1038/s41396-021-01135-1, 2021.
Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N., and Dunne, J. P.:
Spatial coupling of nitrogen inputs and losses in the ocean, Nature, 445,
163–167, https://doi.org/10.1038/nature05392, 2007.
Ding, C., Wu, C., Li, L., Pujari, L., Zhang, G., and Sun, J.: Comparison of
diazotrophic composition and distribution in the South China Sea and the
Western Pacific Ocean, Biology, 10, 555, https://doi.org/10.3390/biology10060555, 2021.
Farnelid, H., Tarangkoon, W., Hansen, G., Hansen, P. J., and Riemann, L.:
Putative N2-fixing heterotrophic bacteria associated with
dinoflagellate–cyanobacteria consortia in the low-nitrogen Indian Ocean,
Aquat. Microb. Ecol., 61, 105–117, https://doi.org/10.3354/ame01440, 2010.
Farnelid, H., Andersson, A. F., Bertilsson, S., Abu Al-Soud, W., Hansen, L.
H., Sorensen, S., Steward, G. F., Hagstrom, A., and Riemann, L.: Nitrogenase
gene amplicons from global marine surface waters are dominated by genes of
non-cyanobacteria, PLoS One, 6, e19223, https://doi.org/10.1371/journal.pone.0019223, 2011.
Fernandez, C., Farias, L., and Ulloa, O.: Nitrogen fixation in denitrified
marine waters, PLoS One, 6, 20539, https://doi.org/10.1371/journal.pone.0020539, 2011.
Fong, A. A., Karl, D. M., Lukas, R., Letelier, R. M., Zehr, J. P., and
Church, M. J.: Nitrogen fixation in an anticyclonic eddy in the oligotrophic
North Pacific Ocean, ISME J., 2, 663–676, https://doi.org/10.1038/ismej.2008.22, 2008.
Gaube, P., McGillicuddy Jr., D. J., Chelton, D. B., Behrenfeld, M. J., and
Strutton, P. G.: Regional variations in the influence of mesoscale eddies on
near-surface chlorophyll, J. Geophys. Res.-Oceans, 119, 8195–8220, https://doi.org/10.1002/2014JC010111, 2014.
Geisler, E., Bogler, A., Rahav, E., and Bar-Zeev, E.: Direct detection of
heterotrophic diazotrophs associated with planktonic aggregates, Sci. Rep.-UK,
9, 1–9, https://doi.org/10.1038/s41598-019-45505-4, 2019.
Geisler, E., Bogler, A., Bar-Zeev, E., and Rahav, E.: Heterotrophic nitrogen
fixation at the hyper-eutrophic qshon river and estuary system, Front.
Microbiol., 11, 1370, https://doi.org/10.3389/fmicb.2020.01370,
2020.
Glover, D. M., Jenkins, W. J., and Doney, S. C.: Modeling methods for marine
science, Cambridge University Press, Cambridge, UK, https://doi.org/10.1017/CBO9780511975721, 2011.
Gradoville, M. R., Bombar, D., Crump, B. C., Letelier, R. M., Zehr, J. P.,
and White, A. E.: Diversity and activity of nitrogen-fixing communities
across ocean basins, Limnol. Oceanogr., 62, 1895–1909, https://doi.org/10.1002/lno.10542, 2017.
Halm, H., Lam, P., Ferdelman, T. G., Lavik, G., Dittmar, T., LaRoche, J.,
D'Hondt, S., and Kuypers, M. M. M.: Heterotrophic organisms dominate
nitrogen fixation in the South Pacific Gyre, ISME J., 6, 1238–1249,
https://doi.org/10.1038/ismej.2011.182, 2012.
Hamersley, M. R., Turk, K. A., Leinweber, A., Gruber, N., Zehr, J. P.,
Gunderson, T., and Capone, D. G.: Nitrogen fixation within the water column
associated with two hypoxic basins in the Southern California Bight, Aquat.
Microb. Ecol., 63, 193–205, https://doi.org/10.3354/ame01494,
2011.
Jayakumar, A. and Ward, B. B.: Diversity and distribution of nitrogen fixation genes in the oxygen minimum zones of the world oceans, Biogeosciences, 17, 5953–5966, https://doi.org/10.5194/bg-17-5953-2020, 2020.
Karl, D., Michaels, A., Bergman, B., Capone, D., Carpenter, E., Letelier,
R., Lipschultz, F., Paerl, H., Sigman, D., and Stal, L.: Dinitrogen fixation
in the world's oceans, Biogeochemistry, 57, 47–98, https://doi.org/10.1023/a:1015798105851, 2002.
Karl, D. M. and Letelier, R. M.: Nitrogen fixation-enhanced carbon
sequestration in low nitrate, low chlorophyll seascapes, Mar. Ecol.-Prog.
Ser., 364, 257–268, https://doi.org/10.3354/meps07547, 2008.
Knapp, A. N., Casciotti, K. L., Berelson, W. M., Prokopenko, M. G., and
Capone, D. G.: Low rates of nitrogen fixation in eastern tropical South
Pacific surface waters, P. Natl. Acad. Sci. USA, 113, 4398–4403, https://doi.org/10.1073/pnas.1515641113, 2016.
Lam, P. and Kuypers, M. M. M.: Microbial nitrogen cycling processes in
oxygen minimum zones, Annu. Rev. Mar. Sci., 3, 317–345, https://doi.org/10.1146/annurev-marine-120709-142814, 2011.
Landolfi, A., Prowe, A. E. F., Pahlow, M., Somes, C. J., Chien, C.-T.,
Schartau, M., Koeve, W., and Oschlies, A.: Can top-down controls expand the
ecological niche of marine N2 fixers?, Front. Microbiol., 12, 690200,
https://doi.org/10.3389/fmicb.2021.690200, 2021.
Langlois, R., Grokopf, T., Mills, M., Takeda, S., and LaRoche, J.:
Widespread distribution and expression of Gamma A (UMB), an uncultured,
diazotrophic, gamma-proteobacterial nifH phylotype, PLoS One, 10, e0128912, https://doi.org/10.1371/journal.pone.0128912, 2015.
Langlois, R. J., Hummer, D., and LaRoche, J.: Abundances and distributions
of the dominant nifH phylotypes in the Northern Atlantic Ocean, Appl. Environ.
Microb., 74, 1922–1931, https://doi.org/10.1128/AEM.01720-07,
2008.
Lee, Z. P., Du, K. P., Arnone, R., Liew, S. C., and Penta, B.: Penetration
of solar radiation in the upper ocean: A numerical model for oceanic and
coastal waters, J. Geophys. Res.-Oceans, 110, C09019, https://doi.org/10.1029/2004jc002780, 2005.
Li, D., Jing, H., Zhang, R., Yang, W., Chen, M., Wang, B., Zheng, M., and
Qiu, Y.: Heterotrophic diazotrophs in a eutrophic temperate bay (Jiaozhou
Bay) broadens the domain of N2 fixation in China's coastal waters,
Estuar. Coast. Mar. Sci., 242, 106778, https://doi.org/10.1016/j.ecss.2020.106778, 2020.
Liu, J. X., Zhou, L. B., Li, J. J., Lin, Y. Y., Ke, Z. X., Zhao, C. Y., Liu,
H. J., Jiang, X., He, Y. H., and Tan, Y. H.: Effect of mesoscale eddies on
diazotroph community structure and nitrogen fixation rates in the South
China Sea, Reg. Stud. Mar. Sci., 35, 101106, https://doi.org/10.1016/j.rsma.2020.101106, 2020.
Loescher, C. R., Großkopf, T., Desai, F. D., Gill, D., Schunck, H.,
Croot, P. L., Schlosser, C., Neulinger, S. C., Pinnow, N., Lavik, G.,
Kuypers, M. M. M., LaRoche, J., and Schmitz, R. A.: Facets of diazotrophy in
the oxygen minimum zone waters off Peru, ISME J., 8, 2180–2192, https://doi.org/10.1038/ismej.2014.71, 2014.
Luo, Y.-W., Lima, I. D., Karl, D. M., Deutsch, C. A., and Doney, S. C.: Data-based assessment of environmental controls on global marine nitrogen fixation, Biogeosciences, 11, 691–708, https://doi.org/10.5194/bg-11-691-2014, 2014.
Marra, G. and Wood, S. N.: Practical variable selection for generalized
additive models, Comput. Stat. Data An., 55, 2372–2387, https://doi.org/10.1016/j.csda.2011.02.004, 2011.
Martínez, L., Silver, M. W., King, J. M., and Alldredge, A. L.:
Nitrogen fixation by floating diatom mats: A source of new nitrogen to
oligotrophic ocean waters, Science, 221, 152–154, https://doi.org/10.1126/science.221.4606.152, 1983.
Martínez-Pérez, C., Mohr, W., Loscher, C. R., Dekaezemacker, J.,
Littmann, S., Yilmaz, P., Lehnen, N., Fuchs, B. M., Lavik, G., Schmitz, R.
A., LaRoche, J., and Kuypers, M. M.: The small unicellular diazotrophic
symbiont, UCYN-A, is a key player in the marine nitrogen cycle, Nat.
Microbiol., 1, 16163, https://doi.org/10.1038/nmicrobiol.2016.163, 2016.
Martínez-Pérez, C., Mohr, W., Schwedt, A., Dürschlag, J.,
Callbeck, C. M., Schunck, H., Dekaezemacker, J., Buckner, C. R., Lavik, G.,
and Fuchs, B. M.: Metabolic versatility of a novel N2-fixing
Alphaproteobacterium isolated from a marine oxygen minimum zone, Environ.
Microbiol., 20, 755–768, https://doi.org/10.1111/1462-2920.14008, 2018.
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.:
Influence of mesoscale eddies on new production in the Sargasso Sea, Nature,
394, 263–266, https://doi.org/10.1038/28367, 1998.
McGillicuddy Jr., D. J.: Mechanisms of physical-biological-biogeochemical
interaction at the oceanic mesoscale, Annu. Rev. Mar. Sci., 8, 125–159,
https://doi.org/10.1146/annurev-marine-010814-015606, 2016.
Misumi, K., Lindsay, K., Moore, J. K., Doney, S. C., Bryan, F. O., Tsumune, D., and Yoshida, Y.: The iron budget in ocean surface waters in the 20th and 21st centuries: projections by the Community Earth System Model version 1, Biogeosciences, 11, 33–55, https://doi.org/10.5194/bg-11-33-2014, 2014.
Moisander, P. H., Beinart, R. A., Voss, M., and Zehr, J. P.: Diversity and
abundance of diazotrophic microorganisms in the South China Sea during
intermonsoon, ISME J., 2, 954–967, https://doi.org/10.1038/ismej.2008.51, 2008.
Moisander, P. H., Serros, T., Paerl, R. W., Beinart, R. A., and Zehr, J. P.:
Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of
the South Pacific Ocean, ISME J., 8, 1962–1973, https://doi.org/10.1038/ismej.2014.49, 2014.
Moisander, P. H., Benavides, M., Bonnet, S., Berman-Frank, I., White, A. E.,
and Riemann, L.: Chasing after non-cyanobacterial nitrogen fixation in
marine pelagic environments, Front. Microbiol., 8, 1736, https://doi.org/10.3389/fmicb.2017.01736, 2017.
Moore, R. M., Grefe, I., Zorz, J., Shan, S., Thompson, K., Ratten, J., and
LaRoche, J.: On the relationship between hydrogen saturation in the tropical
Atlantic Ocean and nitrogen fixation by the symbiotic diazotroph UCYN-A, J.
Geophys. Res.-Oceans, 123, 2353–2362, https://doi.org/10.1002/2017jc013047, 2018.
Moreira-Coello, V., Mourino-Carballido, B., Maranon, E., Fernandez-Carrera,
A., Bode, A., and Varela, M. M.: Biological N2 fixation in the
upwelling region off NW Iberia: magnitude, relevance, and players, Front.
Mar. Sci., 4, 303, https://doi.org/10.3389/fmars.2017.00303,
2017.
Pedersen, J. N., Bombar, D., Paerl, R. W., and Riemann, L.: Diazotrophs and
N2-fixation associated with particles in coastal estuarine waters,
Front. Microbiol., 9, 2759, https://doi.org/10.3389/fmicb.2018.02759, 2018.
Rahav, E., Bar-Zeev, E., Ohayon, S., Elifantz, H., Belkin, N., Herut, B.,
Mulholland, M. R., and Berman-Frank, I.: Dinitrogen fixation in aphotic
oxygenated marine environments, Front. Microbiol., 4, 227, https://doi.org/10.3389/fmicb.2013.00227, 2013.
Rahav, E., Herut, B., Mulholland, M. R., Belkin, N., Elifantz, H., and
Berman-Frank, I.: Heterotrophic and autotrophic contribution to dinitrogen
fixation in the Gulf of Aqaba, Mar. Ecol.-Prog. Ser., 522, 67–77, https://doi.org/10.3354/meps11143, 2015.
Rahav, E., Giannetto, M. J., and Bar-Zeev, E.: Contribution of mono and
polysaccharides to heterotrophic N2 fixation at the eastern
Mediterranean coastline, Sci. Rep.-UK, 6, 27858, https://doi.org/10.1038/srep27858, 2016.
Riemann, L., Farnelid, H., and Steward, G. F.: Nitrogenase genes in
non-cyanobacterial plankton: prevalence, diversity and regulation in marine
waters, Aquat. Microb. Ecol., 61, 225–237, https://doi.org/10.3354/ame01431, 2010.
Robidart, J. C., Church, M. J., Ryan, J. P., Ascani, F., Wilson, S. T., Bombar, D., Marin, R., Richards, K. J., Karl, D. M., Scholin, C. A., and Zehr, J. P.: Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean, ISME J., 8, 1175–1185, https://doi.org/10.1038/ismej.2013.244, 2014.
Roshan, S. and DeVries, T.: Efficient dissolved organic carbon production
and export in the oligotrophic ocean, Nat. Commun., 8, 2036, https://doi.org/10.1038/s41467-017-02227-3, 2017.
Sargent, E. C., Hitchcock, A., Johansson, S. A., Langlois, R., Moore, C. M.,
LaRoche, J., Poulton, A. J., and Bibby, T. S.: Evidence for polyploidy in
the globally important diazotroph Trichodesmium, FEMS Microbiol. Lett., 363, fnw244,
https://doi.org/10.1093/femsle/fnw244, 2016.
Scavotto, R. E., Dziallas, C., Bentzon-Tilia, M., Riemann, L., and
Moisander, P. H.: Nitrogen-fixing bacteria associated with copepods in
coastal waters of the North Atlantic Ocean, Environ. Microbiol., 17,
3754–3765, https://doi.org/10.1111/1462-2920.12777, 2015.
Shao, Z. and Luo, Y.-W.: Gamma A nifH abundance in the global ocean, figshare
[data set], https://doi.org/10.6084/m9.figshare.17284517, 2021.
Shiozaki, T., Ijichi, M., Kodama, T., Takeda, S., and Furuya, K.:
Heterotrophic bacteria as major nitrogen fixers in the euphotic zone of the
Indian Ocean, Global Biogeochem. Cy., 28, 1096–1110, https://doi.org/10.1002/2014gb004886, 2014.
Shiozaki, T., Nagata, T., Ijichi, M., and Furuya, K.: Nitrogen fixation and the diazotroph community in the temperate coastal region of the northwestern North Pacific, Biogeosciences, 12, 4751–4764, https://doi.org/10.5194/bg-12-4751-2015, 2015.
Shiozaki, T., Bombar, D., Riemann, L., Hashihama, F., Takeda, S., Yamaguchi,
T., Ehama, M., Hamasaki, K., and Furuya, K.: Basin scale variability of
active diazotrophs and nitrogen fixation in the North Pacific, from the
tropics to the subarctic Bering Sea, Global Biogeochem. Cy., 31, 996–1009,
https://doi.org/10.1002/2017gb005681, 2017.
Shiozaki, T., Kondo, Y., Yuasa, D., and Takeda, S.: Distribution of major
diazotrophs in the surface water of the Kuroshio from northeastern Taiwan to
south of mainland Japan, J. Plankton Res., 40, 407–419, https://doi.org/10.1093/plankt/fby027, 2018a.
Shiozaki, T., Bombar, D., Riemann, L., Sato, M., Hashihama, F., Kodama, T.,
Tanita, I., Takeda, S., Saito, H., Hamasaki, K., and Furuya, K.: Linkage
between dinitrogen fixation and primary production in the oligotrophic South
Pacific Ocean, Global Biogeochem. Cy., 32, 1028–1044, https://doi.org/10.1029/2017gb005869, 2018b.
Smith, C. J. and Osborn, A. M.: Advantages and limitations of quantitative
PCR (Q-PCR)-based approaches in microbial ecology, FEMS Microbiol.
Ecol., 67, 6–20, https://doi.org/10.1111/j.1574-6941.2008.00629.x, 2009.
Smith, C. J., Nedwell, D. B., Dong, L. F., and Osborn, A. M.: Evaluation of
quantitative polymerase chain reaction-based approaches for determining gene
copy and gene transcript numbers in environmental samples, Environ.
Microbiol., 8, 804–815, https://doi.org/10.1111/j.1462-2920.2005.00963.x, 2006.
Sohm, J. A., Webb, E. A., and Capone, D. G.: Emerging patterns of marine
nitrogen fixation, Nat. Rev. Microbiol., 9, 499–508, https://doi.org/10.1038/nrmicro2594, 2011.
Tréguer, P., Bowler, C., Moriceau, B., Dutkiewicz, S., Gehlen, M.,
Aumont, O., Bittner, L., Dugdale, R., Finkel, Z., Iudicone, D., Jahn, O.,
Guidi, L., Lasbleiz, M., Leblanc, K., Levy, M., and Pondaven, P.: Influence
of diatom diversity on the ocean biological carbon pump, Nat. Geosci., 11,
27–37, https://doi.org/10.1038/s41561-017-0028-x, 2018.
Turk-Kubo, K. A., Karamchandani, M., Capone, D. G., and Zehr, J. P.: The
paradox of marine heterotrophic nitrogen fixation: abundances of
heterotrophic diazotrophs do not account for nitrogen fixation rates in the
Eastern Tropical South Pacific, Environ. Microbiol., 16, 3095–3114, https://doi.org/10.1111/1462-2920.12346, 2014.
Wang, H. and Luo, Y.-W.: Top-down control on major groups of global marine
diazotrophs, Acta Oceanol. Sin., in press, 41, https://doi.org/10.1007/s13131-021-1956-2, 2022.
Wang, W. L., Moore, J. K., Martiny, A. C., and Primeau, F. W.: Convergent
estimates of marine nitrogen fixation, Nature, 566, 205–213, https://doi.org/10.1038/s41586-019-0911-2, 2019.
White, A. E., Watkins-Brandt, K. S., and Church, M. J.: Temporal variability
of Trichodesmium spp. and diatom-diazotroph assemblages in the North Pacific subtropical
gyre, Front. Mar. Sci., 5, 27, https://doi.org/10.3389/fmars.2018.00027, 2018.
Wiebe, P. H. and Joyce, T. M.: Introduction to interdisciplinary studies of
Kuroshio and Gulf Stream rings, Deep-Sea Res. Pt. A, 39, v–vi, https://doi.org/10.1016/S0198-0149(11)80001-4, 1992.
Wood, S. N.: Generalized additive models: an introduction with R, CRC press, https://doi.org/10.1201/9781315370279,
2017.
Wood, S. N., Pya, N., and Säfken, B.: Smoothing parameter and model
selection for general smooth models, J. Am. Stat. Assoc., 111, 1548–1563,
https://doi.org/10.1080/01621459.2016.1180986, 2016.
Wu, C., Kan, J., Liu, H., Pujari, L., Guo, C., Wang, X., and Sun, J.:
Heterotrophic bacteria dominate the diazotrophic community in the Eastern
Indian Ocean (EIO) during pre-southwest monsoon, Microb. Ecol., 78, 804–819,
https://doi.org/10.1007/s00248-019-01355-1, 2019.
Zehr, J. P.: Nitrogen fixation by marine cyanobacteria, Trends Microbiol.,
19, 162–173, https://doi.org/10.1016/j.tim.2010.12.004, 2011.
Zehr, J. P. and Capone, D. G.: Changing perspectives in marine nitrogen
fixation, Science, 368, eaay9514, https://doi.org/10.1126/science.aay9514, 2020.
Zehr, J. P. and Kudela, R. M.: Nitrogen cycle of the open ocean: from genes
to ecosystems, Annu. Rev. Mar. Sci., 3, 197–225, https://doi.org/10.1146/annurev-marine-120709-142819, 2011.
Zehr, J. P., Jenkins, B. D., Short, S. M., and Steward, G. F.: Nitrogenase
gene diversity and microbial community structure: a cross-system comparison,
Environ. Microbiol., 5, 539–554, https://doi.org/10.1046/j.1462-2920.2003.00451.x, 2003.
Zhang, Y., Zhao, Z., Sun, J., and Jiao, N.: Diversity and distribution of
diazotrophic communities in the South China Sea deep basin with mesoscale
cyclonic eddy perturbations, FEMS Microbiol. Ecol., 78, 417–427,
https://doi.org/10.1111/j.1574-6941.2011.01174.x, 2011.
Short summary
Non-cyanobacterial diazotrophs (NCDs) may be an important player in fixing N2 in the ocean. By conducting meta-analyses, we found that a representative marine NCD phylotype, Gamma A, tends to inhabit ocean environments with high productivity, low iron concentration and high light intensity. It also appears to be more abundant inside cyclonic eddies. Our study suggests a niche differentiation of NCDs from cyanobacterial diazotrophs as the latter prefers low-productivity and high-iron oceans.
Non-cyanobacterial diazotrophs (NCDs) may be an important player in fixing N2 in the ocean. By...
Altmetrics
Final-revised paper
Preprint