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Nitrate assimilation by marine heterotrophic bacteria

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Abstract

Nitrate assimilation is a process where bacteria utilize nitrate as a nitrogen source and synthesize it into organic nitrogen. We found that nitrate-assimilating bacteria (NAB) are widely distributed in various marine environments, from surface to the deep ocean and sediment, which indicates that NAB are significant to the oceanic nitrogen cycle. Comparative genomic analysis revealed nitrate-assimilating genes (nasA) in these marine heterotrophic NAB showed different gene arrangements and diverse regulation systems. Summary on recent findings will contribute to understanding the process of nitrate assimilation in NAB and their ecological significance in the nitrogen cycle. A systematic analysis of a number of studies on bacterial nitrate assimilation in marine ecological systems was conducted to clarify directions for future research.

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References

  • Allen A E, Booth M G, Verity P G, Frischer M E. 2005. Influence of nitrate availability on the distribution and abundance of heterotrophic bacterial nitrate assimilation genes in the Barents Sea during summer. Aquat Microbiol Ecol, 39: 247–255

    Article  Google Scholar 

  • Allen A E, Booth M G, Frischer M E, Verity P G, Zehr J P, Zani S. 2001. Diversity and detection of nitrate assimilation genes in marine bacteria. Appl Environ Microbiol, 67: 5343–5348

    Article  Google Scholar 

  • Allen A E, Howard-Jones M H, Booth M G, Frischer M E, Verity P G. Bronk D A, Sanderson M P. 2002. Importance of heterotrophic bacterial assimilation of ammonium and nitrate in the Barents Sea during summer. J Marine Syst, 38: 93–108

    Article  Google Scholar 

  • Andersson M G, Van Rijswijk P, Middelburg J J. 2006. Uptake of dissolved inorganic nitrogen, urea and amino acids in the Scheldt estuary: Comparison of organic carbon and nitrogen uptake. Aquat Microbiol Ecol, 44: 303–315

    Article  Google Scholar 

  • Bao P, Huang H, Hu Z Y, Haggblom M M, Zhu Y G. 2012. Impact of temperature, CO2 fixation and nitrate reduction on selenium reduction, by a paddy soil Clostridium strain. J Appl Microbiol, 113: doi: 10.1111/jam.12084

    Google Scholar 

  • Bradley P B, Sanderson M P, Frischer M E, Brofft J, Booth M G, Kerkhof L J, Bronk D A. 2010. Inorganic and organic nitrogen uptake by phytoplankton and heterotrophic bacteria in the stratified Mid-Atlantic Bight. Estuar Coast Shelf S, 88: 429–441

    Article  Google Scholar 

  • Bronk D, Ward B. 2005. Inorganic and organic nitrogen cycling in the Southern California Bight. Deep-Sea Res Part I-Oceanogr Res Pap, 52: 2285–2300

    Article  Google Scholar 

  • Cai H Y, Jiao N Z. 2008. Diversity and Abundance of Nitrate Assimilation Genes in the Northern South China Sea. Microbiol Ecol, 56: 751–764

    Article  Google Scholar 

  • Cho B C, Azam F. 1988. Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature, 332: 441–443

    Article  Google Scholar 

  • Cochlan W P, Bronk D A. 2003. Effects of ammonium on nitrate utilization in the Ross Sea, Antarctica: Implications for f-ratio estimates. Biogeochem Ross Sea, 78: 159–178

    Article  Google Scholar 

  • Dugdale R C, Goering J J. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr, 12: 196–206

    Article  Google Scholar 

  • Eberl L, Ammendola A, Rothballer M H, Givskov M, Sternberg C, Kilstrup M, Schleifer K H, Molin S. 2000. Inactivation of gltB abolishes expression of the assimilatory nitrate reductase gene (nasB) in Pseudomonas putida KT2442. J Bacteriol, 182: 3368–3376

    Article  Google Scholar 

  • Eppley R, Sharp J, Renger E, Perry M, Harrison W. 1977. Nitrogen assimilation by phytoplankton and other microorganisms in the surface waters of the central North Pacific Ocean. Mar Biol, 39: 111–120

    Article  Google Scholar 

  • Fouilland E, Gosselin M, Rivkin RB, Vasseur C, Mostajir B. 2007. Nitrogen uptake by heterotrophic bacteria and phytoplankton in Arctic surface waters. J Plankton Res, 29: 369–376

    Article  Google Scholar 

  • Fowler D, Coyle M, Skiba U, Sutton M A, Cape J N, Reis S, Sheppard L J, Jenkins A, Grizzetti B, Galloway J N, Vitousek P, Leach A, Bouwman A F, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M. 2013. The global nitrogen cycle in the twenty-first century. Philos Trans R Soc B-Biol Sci, 368: 20130164

    Article  Google Scholar 

  • Gonzalez P J, Correia C, Moura I, Brondino C D, Moura J J. 2006. Bacterial nitrate reductases: Molecular and biological aspects of nitrate reduction. J Inorg Biochem, 100: 1015–1023

    Article  Google Scholar 

  • Gorfer M, Blumhoff M, Klaubauf S, Urban A, Inselsbacher E, Bandian D, Mitter B, Sessitsch A, Wanek W, Strauss J. 2011. Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. ISME J, 5: 1771–1783

    Article  Google Scholar 

  • Harrison W, Wood L J. 1988. Inorganic nitrogen uptake by marine picoplankton: Evidence for size partitioning. Limnol Oceanogr, 33: 468–475

    Article  Google Scholar 

  • Hille R. 1996. The mononuclear molybdenum enzymes. Chem Rev, 96: 2757–2816

    Article  Google Scholar 

  • Jiang X, Dang H, Jiao N. 2015. Ubiquity and diversity of heterotrophic bacterial nasA genes in diverse marine environments. PloS one, 10: e0117473

    Article  Google Scholar 

  • Jiao N Z. 2012. Carbon fixation and sequestration in the ocean, with special reference to the microbial carbon pump (in Chinese). Sci Sin Terrae, 42: 1473–1486

    Google Scholar 

  • Jiao N, Tang K, Cai H, Mao Y. 2010. Increasing the microbial carbon sink in the sea by reducing chemical fertilization on the land. Nat Rev Microbiol, 9: 75–75

    Article  Google Scholar 

  • Kirchman D L, Wheeler P A. 1998. Uptake of ammonium and nitrate by heterotrophic bacteria and phytoplankton in the sub-Arctic Pacific. Deep-Sea Res Part I-Oceanogr Res Pap, 45: 347–365

    Article  Google Scholar 

  • Kirchman D L, Suzuki Y, Garside C, Ducklow H W. 1991. High turnover rates of dissolved organic carbon during a spring phytoplankton bloom. Nature, 352: 612–614

    Article  Google Scholar 

  • Kirchman D L, Ducklow H W, McCarthy J J, Garside C. 1994. Biomass and nitrogen uptake by heterotrophic bacteria during the spring phytoplankton bloom in the North Atlantic Ocean. Deep-Sea Res Part I-Oceanogr Res Pap, 41: 879–895

    Article  Google Scholar 

  • Kraft B, Tegetmeyer H E, Sharma R, Klotz M G, Ferdelman T G, Hettich R L, Geelhoed J S, Strous M. 2014. The environmental controls that govern the end product of bacterial nitrate respiration. Science, 345: 676–679

    Article  Google Scholar 

  • Lam P, Lavik G, Jensen M M, Vossenberg J, Schmid M, Woebken D, Gutierrez D, Amann R, Jetten M S and Kuypers M M. 2009. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Nalt Acad Sci USA, 106: 4752–4757

    Article  Google Scholar 

  • Lledo B, Marhuenda-Egea F C, Martinez-Espinosa R M, Bonete M J. 2005. Identification and transcriptional analysis of nitrate assimilation genes in the halophilic archaeon Haloferax mediterranei. Gene, 361: 80–88

    Article  Google Scholar 

  • Luque-Almagro V M, Gates A J, Moreno-Vivian C, Ferguson S J, Richardson D J, Roldan M D. 2011. Bacterial nitrate assimilation: Gene distribution and regulation. Biochem Soc T, 39: 1838–1843

    Article  Google Scholar 

  • Martinez-Espinosa R M, Marhuenda-Egea F C, Bonete M J. 2001. Assimilatory nitrate reductase from the haloarchaeon Haloferax mediterranei: Purification and characterisation. FEMS Microbiol Lett, 204: 381–385

    Article  Google Scholar 

  • Middelburg J J, Nieuwenhuize J. 2000. Nitrogen uptake by heterotrophic bacteria and phytoplankton in the nitrate rich Thames estuary. Mar Ecol Prog Ser, 203: 13–21

    Article  Google Scholar 

  • Moreno-Vivian C, Cabello P, Martinez-Luque M, Blasco R, Castillo F. 1999. Prokaryotic Nitrate Reduction: Molecular Properties and Functional Distinction among Bacterial Nitrate Reductases. Am Soc Microbiol, 181: 6573–6584

    Google Scholar 

  • Nogales B, Timmis K N, Nedwell D B, Osborn A M. 2002. Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol, 68: 5017–5025

    Article  Google Scholar 

  • Noriega C, Hassett D J, Rowe J J. 2005. The mobA gene is required for assimilatory and respiratory nitrate reduction but not xanthine dehydrogenase activity in Pseudomonas aeruginosa. Curr Microbiol, 51: 419–424

    Article  Google Scholar 

  • Probyn T. 1985. Nitrogen uptake by size-fractionated phytoplankton populations in the southern Benguela upwelling system. Mar Ecol Prog Ser, 22: 249–258

    Article  Google Scholar 

  • Qu H J, Kroeze C. 2011. Nutrient export by rivers to the coastal waters of China: Management strategies and future trends. Reg Environ Change, 1: 153–167

    Google Scholar 

  • Richardson D J, Berks B C, Russell D A, Spiro S, Taylor C J. 2001. Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci, 58: 165–178

    Article  Google Scholar 

  • Rodrigues R M N V, Williams P J L. 2002. Inorganic nitrogen assimilation by picoplankton and whole plankton in a coastal ecosystem. Limnol Oceanogr, 47: 1608–1616

    Article  Google Scholar 

  • Sanderson M P, Bronk D A, Nejstgaard J C, Verity P G, Sazhin A F, Frischer M E. 2008. Phytoplankton and bacterial uptake of inorganic and organic nitrogen during an induced bloom of Phaeocystis pouchetii. Aquat Microbiol Ecol, 51: 153–168

    Article  Google Scholar 

  • Solomonson L P, Barber M J. 1990. Assimilatory nitrate reductase: Functional properties and regulation. Annu Rev Plant Biol, 41: 225–253

    Article  Google Scholar 

  • Stepanauskas R, Sieracki M E. 2007. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc Natl Acad Sci USA, 104: 9052–9057

    Article  Google Scholar 

  • Stolz J F, Basu P. 2002. Evolution of nitrate reductase: Molecular and structural variations on a common function. Chembiochem, 3: 198–206

    Article  Google Scholar 

  • Tupas L M, Koike I, Karl D M, Holm-Hansen O. 1994. Nitrogen metabolism by heterotrophic bacterial assemblages in Antarctic coastal waters. Polar Biol, 14: 195–204

    Article  Google Scholar 

  • Ward B B, Devol A H, Rich J J, Chang B X, Bulow S E, Naik H, Pratihary A, Jayakumar A. 2009. Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature, 461: 78–81

    Article  Google Scholar 

  • Wawrik B, Boling W B, Van Nostrand J D, Xie J, Zhou J, Bronk D A. 2012. Assimilatory nitrate utilization by bacteria on the West Florida Shelf as determined by stable isotope probing and functional microarray analysis. FEMS Microbiol Ecol, 79: 400–411

    Article  Google Scholar 

  • Wemheuer B, Güllert S, Billerbeck S, Giebel H A, Voget S, Simon M, Daniel R. 2014. Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol Ecol, 87: 378–389

    Article  Google Scholar 

  • Wheeler P A, Kirchman D L. 1986. Utilization of inorganic and organic nitrogen by bacteria in marine systems. Limnol Oceanogr, 31: 998–1009

    Article  Google Scholar 

  • Yuan X, Glibert P M, Xu J, Liu H, Chen M, Liu H, Yin K, Harrison P J. 2011. Inorganic and organic nitrogen uptake by phytoplankton and bacteria in Hong Kong waters. Estuar Coast, 35: 325–334

    Article  Google Scholar 

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Correspondence to NianZhi Jiao.

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Jiang, X., Jiao, N. Nitrate assimilation by marine heterotrophic bacteria. Sci. China Earth Sci. 59, 477–483 (2016). https://doi.org/10.1007/s11430-015-5212-5

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