Nitrogenase expression in estuarine bacterioplankton influenced by organic carbon and availability of oxygen

FEMS Microbiology Letters

Volumn 362, Issue 14, 2015, Pages

  Severin, Ina ^a,c   Bentzon Tilia, Mikkel ^a,d   Moisander, Pia H ^b   Riemann, Lasse ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

^c LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Bacterial activity; Limiting factors; Nitrogen fixation

Indexed keywords

NITROGENASE; ORGANIC CARBON; OXYGEN; WATER; CARBON; NITROGENASE REDUCTASE; OXIDOREDUCTASE; SEA WATER;

AMPLICON; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPLANKTON; BIOSYNTHESIS; CONTROLLED STUDY; DENMARK; ENVIRONMENTAL FACTOR; EPSILONPROTEOBACTERIA; ESTUARINE SPECIES; GAMMAPROTEOBACTERIA; GENE EXPRESSION; GENE SEQUENCE; HETEROZYGOTE; MICROBIAL COMMUNITY; NITROGENASE GENE; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECIES COMPOSITION; BACTERIUM; ESTUARY; GENETICS; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGY; NITROGEN FIXATION; PHYLOGENY; PHYSIOLOGY; PLANKTON; REAL TIME POLYMERASE CHAIN REACTION;

BACTERIA; CARBON; EPSILONPROTEOBACTERIA; ESTUARIES; GAMMAPROTEOBACTERIA; MICROBIAL CONSORTIA; NITROGEN FIXATION; NITROGENASE; OXIDOREDUCTASES; OXYGEN; PHYLOGENY; PLANKTON; REAL-TIME POLYMERASE CHAIN REACTION; SEAWATER;

EID: 84949033702     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1093/femsle/fnv105     Document Type: Article

References (35)

1. Bentzon-Tilia M, Traving SJ, Mantikci M, et al. Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 2015a;9:273-85.
2. Bentzon-Tilia M, Severin I, Hansen LH, et al. Genomics and ecophysiology of heterotrophic nitrogen fixing bacteria isolated from estuarine surface water. mBIO 2015b;6:e00929-15.
3. Berg OG, Kurland CG. Evolution ofmicrobial genomes: sequence acquisition and loss. Mol Biol Evol 2002;19:2265-76.
4. Capone DG, Zehr JP, Paerl HW, et al. Trichodesmium, a globally significant marine cyanobacterium. Science 1997;176:1221-9.
5. Cauwet G. Determination of dissolved organic carbon (DOC) and nitrogen (DON) by high temperature combustion. In: Grasshoff K, Kremling K, Erhard M (eds) Methods of Seawater Analyses. Weinheim: Wiley-VCH, 1999, 407-20.
6. Farnelid H, Andersson AF, Bertilsson S, et al. Nitrogenase gene amplicons fromglobal marine surface waters are dominated by genes of non-cyanobacteria. PLoS One 2011;6:e19223.
7. Fuhrman JA, Azam F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters - evaluation and field results. Mar Biol 1982;66:109-20.
8. Gasol JM, DelGiorgio PA. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacteria communities. Sci Mar 2000;64:197-224.
9. Goto M, Ando S, Hachisuka Y, et al. Contamination of diverse nifH and nifH-like DNA into commercial PCR primers. FEMS Microbiol Lett 2005;246:33-8.
10. Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4. 2001. http://palaeo-electronica.org/2001 1/past/issue1 01.htm.
11. Hitchcock JN, Mitrovic SM. Different resource limitation by carbon, nitrogen and phosphorus between base flow and high flowconditions for estuarine bacteria and phytoplankton. Estuar Coast Shelf S 2013;135:106-15.
12. Hoikkala L, Aamos H, Lignell R. Changes in nutrient and carbon availability and temperature as factors controlling bacterial growth in the Northern Baltic Sea. Estuar Coast 2009;32:720-33.
13. Holmes RM, Aminot A, Kérouel R, et al. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 1999;56:1801-8.
14. Howarth RE, Marino R, Lane J, et al. Nitrogen-fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol Oceanogr 1988;33:669-87.
15. LaRoche J, Breitbarth E. Importance of the diazotrophs as a source of new nitrogen in the ocean. J Sea Res 2005;53:67-91.
16. Lee S, Fuhrman JA. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microb 1987;53:1298-303.
17. Man-Aharonovich D, Kress N, Bar Zeev E, et al. Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environ Microbiol 2007;9:2354-63.
18. Meyer F, Paarman D, D'Souza M, et al. The metagenomic RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008;9:386-93.
19. Moisander PH, Morrison AE, Ward BB, et al. Spatial-temporal variability in diazotroph assemblages in Chesapeake Bay using an oligonucleotide nifH microarray. Environ Microbiol 2007;9:1823-35.
20. Moisander PH, Serros T, Paerl RW, et al. Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean. ISME J 2014;8:1962-73.
21. Moisander PH, Shiue L, Steward GF, et al. Application of a nifH oligonucleotidemicroarray for profiling diversity of N2 fixing microorganisms in marine microbial mats. Environ Microbiol 2006;8:1721-35.
22. Oksanen J, Guillaume BF, Kindt R, et al. vegan: Community Ecology Package. R package version 2.0-4. 2012. http://vegan.r-forge.r-project.org/.
23. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2008. ISBN:3-900051-07-0, http://www.R-project.org.
24. Riemann B, Bjørnsen PK, Newell S, et al. Calculation of cell production of coastal marine bacteria based on measured incorporation of [3H]thymidine. Limnol Oceanogr 1987;32:471-6.
25. Riemann L, Farnelid H, Steward GF. Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat Microb Ecol 2010;61: 225-37.
26. Schloss PD, Westcott SL, Ryabin T, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 2009;75:7537-41.
27. Short SM, Jenkins BD, Zehr JP. Spatial and temporal distribution of two diazotrophic bacteria in the Chesapeake Bay. Appl Environ Microb 2004;70:2186-92.
28. Smith DC, Azam F. A simple, economical method for measuring bacterial protein synthesis rates in seawater using tritiatedleucine. Mar Microb Food Webs 1992;6:107-14.
29. Turk KA, Rees AP, Zehr JP, et al. Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J 2011;5:1201-12.
30. Turk-Kubo KA, KaramchandaniM, Capone DG, et al. The paradox of marine heterotrophic nitrogen fixation: abundance of heterotrophic diazotrophs do not account for nitrogen fixation rates in the Eastern Tropical South Pacific. Environ Microbiol 2014;16:3095-114.
31. Zehr JP, Crumbliss LL, Church MJ, et al. Nitrogenase genes in PCR and RT-PCR reagents: implications for studies of diversity of functional genes. Biotechniques 2003;35:996-1005.
32. Zehr JP, McReynolds LA. Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microb 1989;55:2522-6.
33. Zehr JP, Turner PJ. Nitrogen fixation: nitrogenase genes and gene expression. In: Paul JH (ed.) Methods in Microbiology. NY: Academic Press, 2001, 271-85.
34. Zehr JP, Waterbury JB, Turner PJ, et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 2001;412:635-8.
35. Zhang L, Hurek T, Reinhold-Hurek B. A nifH-based oligonucleotide microarray for functional diagnostics of nitrogenfixing microorganisms. Microb Ecol 2007;53:456-70.