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Distinctive tasks of different cyanobacteria and associated bacteria in carbon as well as nitrogen fixation and cycling in a late stage Baltic Sea bloom


Autoři: Falk Eigemann aff001;  Angela Vogts aff001;  Maren Voss aff001;  Luca Zoccarato aff002;  Heide Schulz-Vogt aff001
Působiště autorů: Department of Biological Oceanography, Leibniz Institute for Baltic Sea Research Warnemünde, Rostock, Germany aff001;  Department of Stratified Lakes, Leibniz-Institute for Freshwater Ecology and Inland Fisheries, Stechlin, Germany aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223294

Souhrn

Cyanobacteria and associated heterotrophic bacteria hold key roles in carbon as well as nitrogen fixation and cycling in the Baltic Sea due to massive cyanobacterial blooms each summer. The species specific activities of different cyanobacterial species as well as the N- and C-exchange of associated heterotrophic bacteria in these processes, however, are widely unknown. Within one time series experiment we tested the cycling in a natural, late stage cyanobacterial bloom by adding 13C bi-carbonate and 15N2, and performed sampling after 10 min, 30 min, 1 h, 6 h and 24 h in order to determine the fixing species as well as the fate of the fixed carbon and nitrogen in the associations. Uptake of 15N and 13C isotopes by the most abundant cyanobacterial species as well as the most abundant associated heterotrophic bacterial groups was then analysed by NanoSIMS. Overall, the filamentous, heterocystous species Dolichospermum sp., Nodularia sp., and Aphanizomenon sp. revealed no or erratic uptake of carbon and nitrogen, indicating mostly inactive cells. In contrary, non-heterocystous Pseudanabaena sp. dominated the nitrogen and carbon fixation, with uptake rates up to 1.49 ± 0.47 nmol N h-1 l-1 and 2.55 ± 0.91 nmol C h-1 l-1. Associated heterotrophic bacteria dominated the subsequent nitrogen remineralization with uptake rates up to 1.2 ± 1.93 fmol N h-1 cell -1, but were also indicative for fixation of di-nitrogen.

Klíčová slova:

Bacteria – Cyanobacteria – DNA filter assay – Host cells – Phytoplankton – Scanning electron microscopy – Nitrogen fixation – Baltic Sea


Zdroje

1. Wasmund N. Occurrence of cyanobacterial blooms in the Baltic Sea in relation to environmental conditions. Int Rev der gesamten Hydrobiol und Hydrogr. 1997;82: 169–184. doi: 10.1002/iroh.19970820205

2. Wasmund N, Voss M, Lochte K. Evidence of nitrogen fixation by non-heterocystous cyanobacteria in the Baltic Sea and re-calculation of a budget of nitrogen fixation. Mar Ecol Prog Ser. 2001;214: 1–14. doi: 10.3354/meps214001

3. Stal LJ, Staal M, Villbrandt M. Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquat Microb Ecol. 1999;18: 165–173.

4. Bianchi TS, Westman P, Rolff C. Cyanobacterial blooms in the Baltic Sea: Natural or human induced? Limnol Oceanogr. 2000;43: 716–726.

5. Stolte W, Balode M, Carlsson P, Grzebyk D, Janson S, Lips I, et al. Stimulation of nitrogen-fixing cyanobacteria in a Baltic Sea plankton community by land-derived organic matter or iron addition. Mar Ecol Prog Ser. 2006;327: 71–82.

6. Wasmund N, Nausch G, Schneider B, Nagel K, Voss M. Comparison of nitrogen fixation rates determined with different methods: a study in the Baltic Proper. Mar Ecol Prog Ser. 2005;297: 23–31.

7. Ploug H, Musat N, Adam B, Moraru CL, Lavik G, Vagner T, et al. Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea. ISME J. 2010;4: 1215–23. doi: 10.1038/ismej.2010.53 20428225

8. Ohlendieck U, Stuhr A, Siegmund H. Nitrogen fixation by diazotrophic cyanobacteria in the Baltic Sea and transfer of the newly fixed nitrogen to picoplankton organisms. J Mar Syst. 2000;25: 213–219. doi: 10.1016/S0924-7963(00)00016-6

9. Cole JJ. Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst. 1982;13: 291–314.

10. Ramanan R, Kang Z, Kim B, Cho D, Jin L, Oh H, et al. Phycosphere bacterial diversity in green algae reveals an apparent similarity across habitats. ALGAL. 2015;8: 140–144. doi: 10.1016/j.algal.2015.02.003

11. Seymour JR, Amin SA, Raina J-B, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2: 17065. doi: 10.1038/nmicrobiol.2017.65 28555622

12. Walsby AE, Hayes PK, Boje R, Walsby AE, Hayes PK, Boje R. The gas vesicles, buoyancy and vertical distribution of cyanobacteria in the Baltic Sea. Eur J Phycol. 1995;30: 87–94. doi: 10.1080/09670269500650851

13. Bauersachs T, Schouten S, Compaore J, Wollenzien U, Stal LJ, Damste JSS. Nitrogen isotopic fractionation associated with growth on dinitrogen gas and nitrate by cyanobacteria. Limnol Oceanogr. 2009;54: 1403–1411.

14. Klawonn I, Nahar N, Walve J, Andersson B. Cell-specific nitrogen- and carbon-fixation of cyanobacteria in a temperate marine system (Baltic Sea). Environ Microbiol. 2016;18: 4596–4609. doi: 10.1111/1462-2920.13557 27696654

15. Acinas SG, Haverkamp THA, Huisman J, Stal LJ. Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). ISME J. 2009;3: 31–46. doi: 10.1038/ismej.2008.78 18769459

16. Farnelid H, Bentzon-Tilia M, Andersson AF, Bertilsson S, Jost G, Labrenz M, et al. Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J. 2013;7: 1413–23. doi: 10.1038/ismej.2013.26 23446833

17. Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JLS, Markager S, et al. Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J. 2015;9: 273–285. doi: 10.1038/ismej.2014.119 25026373

18. Ploug H, Adam B, Musat N, Kalvelage T, Lavik G, Wolf-Gladrow D, et al. Carbon, nitrogen and O(2) fluxes associated with the cyanobacterium Nodularia spumigena in the Baltic Sea. ISME J. 2011;5: 1549–58. doi: 10.1038/ismej.2011.20 21390075

19. Guillard R. Culture of phytoplankton for feeding marine invertebrates. In: Smith W, Chanley M, editors. Cultur of Marine Invertebrate Animals. 1975. pp. 26–60.

20. Willén T. Studies on the phytoplankton of some lakes connected with or recently isolated from the Baltic. Oikos. 1962;13: 169–199. doi: 10.2307/3565084

21. Weinbauer MG, Fritz I, Wenderoth DF, Höfle MG. Simultaneous extraction from bacterioplankton of total RNA and DNA suitable for quantitative structure and function analyses. Appl Environ Microbiol. 2002;68: 1082–1087. doi: 10.1128/AEM.68.3.1082-1087.2002 11872453

22. Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011;5: 1571–9. doi: 10.1038/ismej.2011.41 21472016

23. Eigemann F, Schulz-Vogt HN. Stable and labile associations of microorganisms with the cyanobacterium Nodularia spumigena. Aquat Microb Ecol. 2019; 3354. https://doi.org/10.3354/ame01918

24. Glöckner FO, Fuchs BM, Glo FO, Amann R. Bacterioplankton compositions of lakes and oceans: a first comparison based on Fluorescence In Situ Hybridization. Appl Environ Microbiol. 1999;65: 3721–3726. 10427073

25. Acinas SG, Ferrera I, Sarmento H, Díez-Vives C, Forn I, Ruiz-González C, et al. Validation of a new catalysed reporter deposition-fluorescence in situ hybridization probe for the accurate quantification of marine Bacteroidetes populations. Environ Microbiol. 2015;17: 3557–3569. doi: 10.1111/1462-2920.12517 24890225

26. Pernthaler A, Pernthaler J, Amann R. Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the identification of marine bacteria. Appl Env Microbiol. 2002;68: 3094–3101. doi: 10.1128/AEM.68.6.3094

27. Musat N, Foster R, Vagner T, Adam B, Kuypers MMM. Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev. 2012;36: 486–511. doi: 10.1111/j.1574-6976.2011.00303.x 22092433

28. Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS—a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14: 1009–1023. doi: 10.1111/j.1462-2920.2011.02681.x 22221878

29. Montoya JP, Voss M, Kahler P, Capone DG. A simple, high-precision, high-sensitivity tracer assay for N(2) fixation. Appl Environ Microbiol. 1996;62: 986–93. 16535283

30. Carpenter J. New measurements of oxygen solubility in pure and natural water. Limnol Oceanogr. 1966;11: 264–277.

31. Weiss R. The solubility of nitrogen, oxygen and argon in water and seawater. Deep Res. 1970;17: 721–735.

32. Sveden JS, Adam B, Walve J, Nahar N, Sved JB, Musat N, et al. High cell-specific rates of nitrogen and carbon fixation by the cyanobacterium Aphanizomenon sp. at low temperatures in the Baltic Sea. FEMS Microbiol Ecol. 2015;91: 1–10. doi: 10.1093/femsec/fiv131 26511856

33. Heinänen AP. Bacterial numbers, biomass and productivity in the Baltic Sea: a cruise study. Mar Ecol Prog Ser. 1991;70: 283–290.

34. Kroer N, Jorgensen NOG, Coffin RB. Utilization of dissolved nitrogen by heterotrophic bacterioplankton: A comparison of three ecosystems. Appl Environ Microbiol. 1994;60: 4116–4123. 16349439

35. Mohr W, Grosskopf T, Wallace DWR, LaRoche J. Methodological underestimation of oceanic nitrogen fixation rates. PLoS One. 2010;5: e12583. doi: 10.1371/journal.pone.0012583 20838446

36. Wannicke N, Benavides M, Dalsgaard T, Dippner JW, Montoya JP, Voss M. New perspectives on nitrogen fixation measurements using 15N2 gas. Front Mar Sci. 2018;5: 1–10. doi: 10.3389/fmars.2018.00043

37. R Development Core Team. R: A language and environment for statistical computing. 2008. Available: http://www.r-project.org/

38. RStudio Team. RStudio: Integrated Development for R. Boston, MA URL http//www.rstudio.com/. 2015.

39. De Mendiburu F. Una herramienta de analisis estadistico para la investigacion agricola. 2009.

40. Oksanen J, Blanchet GF, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community ecology package. 2019.

41. Stal LJ, Albertano P, Bergman B, Von Bröckel K, Gallon JR, Hayes PK, et al. BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea—Responses to a changing environment. Cont Shelf Res. 2003;23: 1695–1714. doi: 10.1016/j.csr.2003.06.001

42. Hesselsoe M, Nielsen JL, Roslev P, Nielsen PH. Isotope labeling and microautoradiography of active heterotrophic bacteria on the basis of assimilation of 14CO2. Appl Environ Microbiol. 2005;71: 646–655. doi: 10.1128/AEM.71.2.646-655.2005 15691913

43. Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, et al. Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J. 2013;7: 1026–1037. doi: 10.1038/ismej.2012.169 23303374

44. Kirchman DL. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39: 91–100. doi: 10.1111/j.1574-6941.2002.tb00910.x 19709188

45. Alonso C, Musat N, Adam B, Kuypers M, Amann R. HISH-SIMS analysis of bacterial uptake of algal-derived carbon in the Rio de la Plata estuary. Syst Appl Microbiol. 2012;35: 541–548. doi: 10.1016/j.syapm.2012.08.004 23026312

46. Mühlenbruch M, Grossart H-P, Eigemann F, Voss M. Phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20: 2671–2685. doi: 10.1111/1462-2920.14302 30028074

47. Seymour JR, Ahmed T, Stocker R. Bacterial chemotaxis towards the extracellular products of the toxic phytoplankton Heterosigma akashiwo. J Plankton Res. 2009;31: 1557–1561. doi: 10.1093/plankt/fbp093

48. Pinhassi J, Havskum H, Peters F, Malits A. Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol. 2004;70: 6753–6766. doi: 10.1128/AEM.70.11.6753-6766.2004 15528542

49. Adam B, Klawonn I, Svedén JB, Bergkvist J, Nahar N, Walve J, et al. N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community. ISME J. 2016;10: 450–459. doi: 10.1038/ismej.2015.126 26262817

50. Farnelid HM, Turk-Kubo KA, Zehr JP. Identification of associations between bacterioplankton and photosynthetic picoeukaryotes in coastal waters. Front Microbiol. 2016;7: 1–16. doi: 10.3389/fmicb.2016.00001

51. Bombar D, Paerl RW, Riemann L. Marine non-cyanobacterial diazotrophs: Moving beyond molecular detection. Trends Microbiol. 2016;24: 916–927. doi: 10.1016/j.tim.2016.07.002 27476748

52. Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, Laroche J, et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J. 2012; 1238–1249. doi: 10.1038/ismej.2011.182 22170429

53. Delmont TO, Quince C, Shaiber A, Esen ÖC, Lee ST, Rappé MS, et al. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat Microbiol. 2018;3: 804–813. doi: 10.1038/s41564-018-0176-9 29891866

54. Inoue J, Oshima K, Suda W, Sakamoto M, Iino T, Noda S, et al. Distribution and evolution of nitrogen fixation genes in the phylum Bacteroidetes. Microbes Environ. 2015;30: 44–50. doi: 10.1264/jsme2.ME14142 25736980

55. Bowman JS, Ducklow HW. Microbial communities can be described by metabolic structure: A general framework and application to a seasonally variable, depth-stratified microbial community from the coastal West Antarctic Peninsula. PLoS One. 2015; 1–18. doi: 10.1371/journal.pone.0135868 26285202

56. Dawson W, Hör J, Egert M, Kleunen M Van, Pester M. A small number of low-abundance bacteria dominate plant species-specific responses during rhizosphere colonization. Front Microbiol. 2017;8: 1–13. doi: 10.3389/fmicb.2017.00001

57. Benjamino J, Lincoln S, Srivastava R, Graf J. Low-abundant bacteria drive compositional changes in the gut microbiota after dietary alteration. Microbiome. 2018; 1–13. doi: 10.1186/s40168-017-0383-2

58. Bonnet S, Dekaezemacker J, Turk-kubo KA, Moutin T, Hamersley RM, Grosso O, et al. Aphotic N2 fixation in the eastern tropical South Pacific Ocean. PLos One. 2013;8: 1–14. doi: 10.1371/journal.pone.0081265 24349048

59. Moisander PH, Steppe TF, Hall NS, Kuparinen J, Paerl HW. Variability in nitrogen and phosphorus limitation for Baltic Sea phytoplankton during nitrogen-fixing cyanobacterial blooms. Mar Ecol Pro Ser. 2003;262: 81–95.

60. Graham LE, Knack JJ, Piotrowski MJ, Wilcox LW, Cook ME, Wellman CH, et al. Lacustrine Nostoc (Nostocales) and associated microbiome generate a new type of modern clotted microbialite. J Phycol. 2014;291: 280–291. doi: 10.1111/jpy.12152

61. Frischkorn KR, Haley ST, Dyhrman ST. Coordinated gene expression between Trichodesmium and its microbiome over day-night cycles in the North Pacific Subtropical Gyre. ISME J. 2018;12: 997–1007. doi: 10.1038/s41396-017-0041-5 29382945

62. Zulkifly S, Hanshew A, Young EB, Lee P, Graham ME, Graham ME, et al. The epiphytic microbiota of the globally widespread macroalga Cladophora glomerata (Chlorophyta, Cladophorales). Am J Bot. 2012;99: 1541–1552. doi: 10.3732/ajb.1200161 22947483


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