Experimental evidence for the role of heterotrophic bacteria in the formation of Microcystis colonies

Journal of Applied Phycology

Volumn 28, Issue 2, 2016, Pages 1111-1123

  Wang, Wenjing ^a,b   Shen, Hong ^a   Shi, Pengling ^c   Chen, Jun ^a   Ni, Leyi ^a   Xie, Ping ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Associated bacteria; Colony formation; Extracellular polysaccharides; Metabolic compounds; Microcystis

Indexed keywords

EID: 84961186576     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-015-0659-5     Document Type: Article

References (61)

1. Adams JH (1978) Synergistic combinations of hydrated potassium borate, antiwear agents, and organic sulfide antioxidants. US Patent 4089790A
2. Armstrong E, Yan L, Boyd KG, Wright PC, Burgess JG (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461:37–40
3. Bell WH (1984) Bacterial adaptation to low-nutrient conditions as studied with algal extracellular products. Microb Ecol 10:217–230
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
5. Bratbak G, Thingstad TF (1985) Phytoplankton-bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism. Mar Ecol Prog Ser 25:23–30
6. Brunberg AK (1999) Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol Ecol 29:13–22
7. Burkert PH, Drakare S, Blomqvist P (2001) Effects of the mixotrophic flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. Aquat Ecol 35:11–17
8. Burton K (1956) A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 62:315
9. Chen W, Peng L, Wan N, Song L (2009) Mechanism study on the frequent variations of cell-bound microcystins in cyanobacterial blooms in Lake Taihu: implications for water quality monitoring and assessments. Chemosphere 77:1585–1593
10. Doucette GJ (1995) Interactions between bacteria and harmful algae: a review. Nat Toxins 3:65–74
11. Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
12. Dziallas C, Grossart HP (2011) Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol 13:1632–1641
13. Forni C, Telo' FR, Caiola MG (1997) Comparative analysis of the polysaccharides produced by different species of Microcystis (Chroococcales, Cyanophyta). Phycologia 36:181–185
14. Giroldo D, Ortolano PI, Vieira AA (2007) Bacteria–algae association in batch cultures of phytoplankton from a tropical reservoir: the significance of algal carbohydrates. Freshw Biol 52:1281–1289
15. Imai A, Fukushima T, Matsushige K (1999) Effects of iron limitation and aquatic humic substances on the growth of Microcystis aeruginosa. Can J Fish Aquat Sci 56:1929–1937
16. Ishikawa K, Walker R, Tsujimura S, Nakahara H, Kumagai M (2004) Estimation of Microcystis colony size in developing water blooms via image analysis. J Jpn Soc Water Environ 4:69–72
17. Ivanovic J, Misic D, Zizovic I, Ristic M (2012) In vitro control of multiplication of some food-associated bacteria by thyme, rosemary and sage isolates. Food Control 25:110–116
18. Jancula D, Marsalek B (2011) Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere 85:1415–1422
19. Joung SH, Kim CJ, Ahn CY, Jang KY, Boo SM, Oh HM (2006) Simple method for a cell count of the colonial cyanobacterium, Microcystis sp. J Microbiol 44:562–565
20. Kessel M, Eloff JN (1975) The ultrastructure and development of the colonial sheath of Microcystis marginata. Arch Microbiol 106:209–214
21. Klock JH, Wieland A, Seifert R, Michaelis W (2007) Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar Biol 152:1077–1085
22. Kolattukudy P (1968) Tests whether a head to head condensation mechanism occurs in the biosynthesis of n-hentriacontane, the paraffin of spinach and pea leaves. Plant Physiol 43:1466
23. Kurmayer R, Christiansen G, Chorus I (2003) The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Appl Environ Microbiol 69:787–795
24. Lee JA, Kontopoulou M, Parent JS (2005) Synthesis and characterization of polyethylene-based ionomer nanocomposites. Polymer 46:5040–5049
25. Lin LH, Chen KM (2006) Preparation and surface activity of gelatin derivative surfactants. Colloids Surf A 272:8–14
26. Liu X, Dong M, Chen X, Jiang M, Lv X, Yan G (2007) Antioxidant activity and phenolics of an endophytic Xylaria sp. from Ginkgo biloba. Food Chem 105:548–554
27. Liu YM, Chen MJ, Wang MH, Jia RB, Li L (2013) Inhibition of Microcystis aeruginosa by the extracellular substances from an Aeromonas sp. J Microbiol Biotechnol 23:1304–1307
28. 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 31:136–142
29. Ma QZ, Wu FJ, Zhang DQ, Peng WX (2011) Py-GC-MS analysis on benzene-alcohol extractives of Phyllostachys pubescens for biomedical engineering. Key Eng Mater 480:211–214
30. Malloy KL, Suyama TL, Engene N, Debonsi H, Cao Z, Matainaho T, Spadafora C, Murray TF, Gerwick WH (2011) Credneramides A and B: neuromodulatory phenethylamine and isopentylamine derivatives of a vinyl chloride-containing fatty acid from cf. Trichodesmium sp. nov. J Nat Prod 75:60–66
31. Manage PM, Kawabata Z, Nakano S-i (2001) Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2:73–78
32. Middelboe M, Søndergaard M, Letarte Y, Borch N (1995) Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb Ecol 29:231–248
33. Mohamed H, Ons M, Yosra ET, Rayda S, Neji G, Moncef N (2009) Chemical composition and antioxidant and radical‐scavenging activities of Periploca laevigata root bark extracts. J Sci Food Agric 89:897–905
34. Nakamura N, Nakano K, Sugiura N, Matsumura M (2003) A novel cyanobacteriolytic bacterium, Bacillus cereus, isolated from a eutrophic lake. J Biosci Bioeng 95:179–184
35. Ngang JEJ et al (2014) Characterization of Mexican coriander (Eryngium foetidum) essential oil and its inactivation of Listeria monocytogenes In vitro and during mild thermal pasteurization of pineapple juice. J Food Protect 77:435–443
36. Parker DL (1982) Improved procedures for the cloning and purification of Microcystis cultures (Cyanophyta) 1. J Phycol 18:471–477
37. Parveen B, Ravet V, Djediat C, Mary I, Quiblier C, Debroas D, Humbert JF (2013) Bacterial communities associated with Microcystis colonies differ from free living communities living in the same ecosystem. Environ Microbiol Rep 5:716–724
38. Pereira S, Zille A, Micheletti E, Moradas‐Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941
39. Plude JL, Parker DL, Schommer OJ, Timmerman RJ, Hagstrom SA, Joers JM, Hnasko R (1991) Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae C3-40. Appl Environ Microbiol 57:1696–1700
40. Porter KG (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948
41. Reynolds CS, Jaworski G, Cmiech H, Leedale G (1981) The formation of colonies or aggregates might be phenotypic response of individuals to current environmental conditions. Phil Trans R Soc B 4:419–477
42. Rippka R (1988) Isolation and purification of cyanobacteria. Method Enzymol 167:3
43. Romo S, Soria J, Fernandez F, Ouahid Y, Barón-Solá Á (2013) Water residence time and the dynamics of toxic cyanobacteria. Freshw Biol 58:513–522
44. Scott JH, Nealson KH (1994) A biochemical study of the intermediary carbon metabolism of Shewanella putrefaciens. J Bacteriol 176:3408–3411
45. Sedmak B, Eleršek T (2006) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 51:508–515
46. Sharman M, Read WA, Castle L, Gilbert J (1994) Levels of di-(2-ethylhexyl) phthalate and total phthalate esters in milk, cream, butter and cheese. Food Addit Contam 11:375–385
47. Shen H, Niu Y, Xie P, Tao M, Yang X (2011) Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshw Biol 56:1065–1080
48. Shi L, Cai Y, Kong F, Yu Y (2012) Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environ Microbiol Rep 4:669–678
49. Shi L, Cai Y, Wang X, Li P, Yu Y, Kong F (2010) Community structure of bacteria associated with Microcystis colonies from cyanobacterial blooms. J Freshw Ecol 25:193–203
50. Shirai M, Matumaru K, Ohotake A, Takamura Y, Aida T, Nakano M (1989) Development of a solid medium for growth and isolation of axenic Microcystis strains (cyanobacteria). Appl Environ Microbiol 55:2569–2571
51. Sundh I (1992) Biochemical composition of dissolved organic carbon derived from phytoplankton and used by heterotrophic bacteria. Appl Environ Microbiol 58:2938–2947
52. Tajima I, Yamamoto M (1987) Characterization of plasma polymers from tetramethylsilane, octamethylcyclotetrasiloxane, and methyltrimethoxysilane. J Polym Sci Polym Chem 25:1737–1744
53. Tian C, Liu X, Tan J, Lin S, Li D, Yang H (2012) Isolation, identification and characterization of an algicidal bacterium from Lake Taihu and preliminary studies on its algicidal compounds. J Environ Sci 24:1823–1831
54. Valdor R, Aboal M (2007) Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon 49:769–779
55. Walker HL, Higginbotham LR (2000) An Aquatic bacterium that lyses cyanobacteria associated with off-flavor of channel catfish Ictalurus punctatus. Biol Control 18:71–78
56. Wang X, Cotter E, Iyer KN, Fang J, Williams BJ, Biswas P (2015) Relationship between pyrolysis products and organic aerosols formed during coal combustion. Proc Combust Inst 35:2347–2354
57. Worm J, Sondergaard M (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14:19–28
58. Wu ZX, Song LR (2008) Physiological comparison between colonial and unicellular forms of Microcystis aeruginosa Kütz. (Cyanobacteria). Phycologia 47:98–104
59. Xu H, Yu G, Jiang H (2013) Investigation on extracellular polymeric substances from mucilaginous cyanobacterial blooms in eutrophic freshwater lakes. Chemosphere 93:75–81
60. Zhang M, Kong FX, Tan X, Yang Z, Cao HS, Xing P (2007) Biochemical, morphological, and genetic variations in Microcystis aeruginosa due to colony disaggregation. World J Microb Biotechnol 23:663–670
61. Zhang P, Zhai C, Wang X, Liu C, Jiang J, Xue Y (2013) Growth competition between Microcystis aeruginosa and Quadrigula chodatii under controlled conditions. J Appl Phycol 25:555–565