Advertisement

Effects of Phosphorus on Interspecific Competition between two cell-size Cyanobacteria: Synechococcus sp. and Microcystis aeruginosa

  • Xiao Tan
  • Huihui Gu
  • Xidong Zhang
  • Keshab Parajuli
  • Zhipeng DuanEmail author
Article

Abstract

Pico-cyanobacteria and micro-cyanobacteria coexist ubiquitously in many lakes. Differences in cell size and abilities to utilize nutrients may influence their distribution patterns. In this study, Synechococcus sp. and Microcystis aeruginosa were chosen as pico- and micro-cyanobacteria, respectively. Gradient phosphorus treatments (0.002, 0.01, 0.05, and 0.25 mg P L−1) were designed in mono- and co-cultures. Growth curves were recorded and fitted by the Monod equation. Moreover, the interspecific competition was analyzed by the Lotka–Volterra model. When mono-cultured in lower P conditions (≤ 0.01 mg P L−1), Synechococcus sp. obtained much higher biomass than M. aeruginosa. But, M. aeruginosa grew faster than Synechococcus sp. in higher P groups (≥ 0.05 mg P L−1) (p < 0.05). Synechococcus sp. has abilities to thrive in low-phosphorus environments, whereas M. aeruginosa favored high-phosphorus conditions. In co-cultures, Synechococcus sp. strongly inhibited M. aeruginosa at each P treatment.

Keywords

Phosphorus Pico-cyanobacteria Micro-cyanobacteria Blooms Biomass Interspecific competition 

Notes

Acknowledgements

This work was supported by National Natural Science Foundation of China (31470507), the Fundamental Research Funds for the Central Universities (2019B14014), the National Water Pollution Control and Treatment Science and Technology Major Project (2017ZX07603) and the project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

References

  1. Barber RT (2007) Picoplankton do some heavy lifting. Science 315:777–778CrossRefGoogle Scholar
  2. Berkson J (1944) Application of the logistic function to bio-assay. J Am Stat Assoc 39:357–365Google Scholar
  3. Björkman K, Duhamel S, Karl DM (2012) Microbial group specific uptake kinetics of inorganic phosphate and adenosine-5′-triphosphate (ATP) in the north Pacific subtropical gyre. Front Microbiol 3:1–17CrossRefGoogle Scholar
  4. Brookes JD, Ganf GG (2001) Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. J Plankton Res 23:1399–1411CrossRefGoogle Scholar
  5. Cade-Menun BJ, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36CrossRefGoogle Scholar
  6. Cai Y, Kong F (2013) Diversity and dynamics of picocyanobacteria and the bloom-forming cyanobacteria in a large shallow eutrophic lake (Lake Chaohu, China). J Limnol 72:473–484CrossRefGoogle Scholar
  7. Callieri C, Caravati E, Corno G, Bertoni R (2012) Picocyanobacterial community structure and space-time dynamics in the subalpine lake Maggiore (Italy). J Limnol 71:95–103CrossRefGoogle Scholar
  8. Danish Standard (2004) Water quality: determination of phosphorus—ammonium molybdate spectrometric method. DS/EN ISO 6878:2004. Danish Standard, CopenhagenGoogle Scholar
  9. Duan Z, Tan X, Parajuli K, Upadhyay S, Zhang D, Shu X, Liu Q (2018) Colony formation in two Microcystis morphotypes: Effects of temperature and nutrient availability. Harmful Algae 72:14–24CrossRefGoogle Scholar
  10. Elshanawany R, Zonneveld KAF (2016) Dinoflagellate cyst distribution in the oligotrophic environments of the Gulf of Aqaba and northern Red Sea. Mar Micropaleontol 124:29–44CrossRefGoogle Scholar
  11. Eppley RW, Rogers JN, Mccarthy JJ (1969) Half saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol Oceanogr 14:912–920CrossRefGoogle Scholar
  12. Feng L, Liu S, Wu W, Ma J, Li P, Xu H, Li N, Feng Y (2016) Dominant genera of cyanobacteria in lake Taihu and their relationships with environmental factors. J Microbiol 54:468–476CrossRefGoogle Scholar
  13. Fukuda R, Ogawa H, Nagata T, Koike II (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358Google Scholar
  14. Fuller NJ, West NJ, Marie D, Yallop M, Rivlin T, Post AF, Scanlan DJ (2005) Dynamics of community structure and P status of picocyanobacterial populations in the Gulf of Aqaba, Red Sea during 1999–2000. Limnol Oceanogr 50:363–375CrossRefGoogle Scholar
  15. Havens KE, Jin KR, Iricanin N (2007) Phosphorus dynamics at multiple time scales in the pelagic zone of a large shallow lake in Florida, USA. Hydrobiologia 581:25–42CrossRefGoogle Scholar
  16. Imai H, Chang K, Kusaba M, Nakano S (2009) Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 31:171–178CrossRefGoogle Scholar
  17. Ji Y, Sherrell RM (2008) Differential effects of phosphorus limitation on cellular metals in Chlorella and Microcystis. Limnol Oceanogr 53:1790–1804CrossRefGoogle Scholar
  18. Karl DM (2002) Nutrient dynamics in the deep blue sea. Trends Microbiol 10:410–418CrossRefGoogle Scholar
  19. Kolmakov VI (2006) Methods for prevention of mass development of the cyanobacterium Microcystis aeruginosa Kutz emend. Elenk. in aquatic ecosystems. Mikrobiologiia 75:149–153Google Scholar
  20. Kolmonen E, Sivonen K, Rapala J, Haukka K (2004) Diversity of cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas Finland. Aquat Microb Ecol 36:201–211CrossRefGoogle Scholar
  21. Latour D, Giraudet H, Berthon JL (2004) Frequency of dividing cells and viability of Microcystis aeruginosa in sediment of a eutrophic reservoir. Aquat Microb Ecol 36:117–122CrossRefGoogle Scholar
  22. Li M, Zhu W, Gao L, Lu L (2013) Changes in extracellular polysaccharide content and morphology of Microcystis aeruginosa at different specific growth rates. J Appl Phycol 25:1023–1030CrossRefGoogle Scholar
  23. Ma J, Brookes JD, Qin B, Paerl HW, Gao G, Wu P, Zhang W, Deng J, Zhu G, Zhang Y, Xu H, Niu H (2014) Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in Lake Taihu, China. Harmful Algae 31:136–142CrossRefGoogle Scholar
  24. Mahaffey C, Björkman KM, Karl DM (2012) Phytoplankton response to deep seawater nutrient addition in the North Pacific Subtropical Gyre. Mar Ecol Prog Ser 460:13–34CrossRefGoogle Scholar
  25. Mao H, Xu H, Liu ZP, Mehta SK (2008) Effect of initial cell density on population competition between Skeletonema costatum and Chaetoceros curvisetus. Mar Environ Sci 27:458–461Google Scholar
  26. Marinho MM, Souza MB, Lurling M (2013) Light and phosphate competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa is strain dependent. Microb Ecol 66:479–488CrossRefGoogle Scholar
  27. Martiny AC, Huang Y, Li W (2009) Occurrence of phosphate acquisition genes in Prochlorococcus, cells from different ocean regions. Environ Microbiol 11:1340–1347CrossRefGoogle Scholar
  28. Monbet P, Mckelvie I, Saefumillah A (2007) A protocol to assess the enzymatic release of dissolved organic phosphorus species in waters under environmentally relevant conditions. Environ Sci Technol 41:7479–7485CrossRefGoogle Scholar
  29. Monod J (1950) La technique de culture continue: théorie et applications. In: Lwoff A, Ullmann A (eds) Selected papers in molecular biology by jacques monod. Academic Press, New York, pp 184–204Google Scholar
  30. Mountain T, Thingstad TF, Wambeke FV, Marie D, Slawyk G, Raimbault P, Claustre H (2002) Does competition for nanomolar phosphate supply explain the predominance of the cyanobacterium Synechococcus?. Limnol Oceanogr 47:1562–1567CrossRefGoogle Scholar
  31. Mulder C, Hendriks AJ (2014) Half-saturation constants in functional responses. Global Ecol Conserv 2:161–169CrossRefGoogle Scholar
  32. Paerl HW (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. Adv Exp Med Biol 619:217–237CrossRefGoogle Scholar
  33. Raven JA (1998) The twelfth tansley lecture, small is beautiful: the picophytoplankton. Funct Ecol 12:503–513CrossRefGoogle Scholar
  34. Riebesell U, Wolf-Gladrow DA (2002) Supply and uptake of inorganic nutrients. In: Williams PJ le Thomas B, Reynolds DN, C.S., (eds) Phytoplankton productivity: carbon assimilation in marine and freshwater ecosystems. Blackwell Science Ltd, Oxford, pp 78–108Google Scholar
  35. Sarmento H, Unrein F, Isumbisho M, Stenuite S, Gasol JM, Descy JP (2008) Abundance and distribution of picoplankton in tropical, oligotrophic Lake Kivu, eastern Africa. Freshw Biol 53:756–771CrossRefGoogle Scholar
  36. Tambi H, Flaten GAF, Egge JK, Bødtker G, Jacobsen A, Thingstad TF (2009) Relationship between phosphate affinities and cell size and shape in various bacteria and phytoplankton. Aquat Microb Ecol 57:311–320CrossRefGoogle Scholar
  37. Vadstein O (2000) Heterotrophic, planktonic bacteria and cycling of phosphorus. Adv Microb Ecol 16:115–167CrossRefGoogle Scholar
  38. Vaulot D, Lebot N, Marie D, Fukai E (1996) Effect of phosphorus on the Synechococcus cell cycle in surface Mediterranean waters during summer. Appl Environ Microb 62:2527–2533Google Scholar
  39. Verity PG (1992) Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr 37:1434–1446CrossRefGoogle Scholar
  40. Vollenweider RA, Kerekes J (1982) Eutrophication of waters. monitoring assessment and control. Organization for Economic Co-Operation and Development (OECD), Paris, 156 ppGoogle Scholar
  41. Volterra V (1926) Fluctuation in the abundance of a species considered mathematically. Nature 118:558–560CrossRefGoogle Scholar
  42. Xiao M, Willis A, Burford MA (2017) Differences in cyanobacterial strain responses to light and temperature reflect species plasticity. Harmful Algae 62:84–93CrossRefGoogle Scholar
  43. Xiao M, Li M, Reynolds CS (2018) Colony formation in the cyanobacterium Microcystis. Biol Rev 93:1399–1420CrossRefGoogle Scholar
  44. Ye W, Tan J, Liu X, Lin S, Pan J, Li D, Yang H (2011) Temporal variability of cyanobacterial populations in the water and sediment samples of Lake Taihu as determined by DGGE and real-time PCR. Harmful Algae 10:472–479CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Xiao Tan
    • 1
  • Huihui Gu
    • 1
  • Xidong Zhang
    • 2
  • Keshab Parajuli
    • 3
  • Zhipeng Duan
    • 1
    Email author
  1. 1.Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes, Ministry of Education, College of EnvironmentHohai UniversityNanjingChina
  2. 2.Nanjing Foreign Language SchoolNanjingChina
  3. 3.Origin Energy LimitedAdelaideAustralia

Personalised recommendations