The epiphytic microbiota of the globally widespread macroalga Cladophora glomerata (Chlorophyta, Cladophorales)

American Journal of Botany

Volumn 99, Issue 9, 2012, Pages 1541-1552

  Zulkifly, Shahrizim ^a   Hanshew, Alissa ^b   Young, Erica B ^c   Lee, Philip ^c   Graham, Melissa E ^d,e   Piotrowski, Michael ^b   Graham, Linda E ^b  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e HOLOGIC INC   (United States)

Author keywords

Alga; Chlorophyta; Cladophora; Cladophorales; Microbiota; Pyrosequencing; Ulvophyceae; Wisconsin

Indexed keywords

RNA 16S;

COLIFORM BACTERIUM; ECOLOGICAL ENGINEERING; EPIPHYTE; EUTROPHICATION; FILAMENTOUS ALGA; FLUORESCENCE SPECTROSCOPY; GREEN ALGA; GROWING SEASON; HOST-PATHOGEN INTERACTION; LAKE ECOSYSTEM; MACROALGA; MICROBIAL COMMUNITY; MUTUALISM; PERIPHYTON; PERSISTENCE; SURFACE AREA;

ARTICLE; BACTERIUM; CLASSIFICATION; GENETICS; GENOTYPE; GREEN ALGA; METAGENOME; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEAWEED; ULTRASTRUCTURE; UNITED STATES;

BACTERIA; BASE SEQUENCE; CHLOROPHYTA; GENOTYPE; METAGENOME; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWEED; WISCONSIN;

DANE COUNTY; LAKE MENDOTA; UNITED STATES; WISCONSIN;

ALGAE; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CLADOPHORA; CLADOPHORA GLOMERATA; CLADOPHORALES; ESCHERICHIA COLI; PROKARYOTA; ULVOPHYCEAE;

EID: 84866134182     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200161     Document Type: Article

References (93)

1. Arancibia-Avila, P., J. R. COLEMAN, W. A. RUSSIN, L. W. WILCOX, J. M. GRAHAM, and L. E. GRAHAM. 2000. Effects of pH on cell morphology and carbonic anhydrase activity and localization in bloom-forming Mougeotia (Chlorophyta, Charophyceae). Canadian Journal of Botany 78: 1206-1214.
2. AUER, M. T., and R. P. CANALE. 1982. Ecological studies and mathematical modeling of Cladophora in Lake Huron: 3. The dependence of growth rates on internal phosphorus pool size. Journal of Great Lakes Research 8: 93-99.
3. AUER, M. T., L. M. TOMLINSON, S. N. HIGGINS, S. Y. MALKIN, E. T. HOWELL, and H. A. BOOTSMA. 2010. Great Lakes Cladophora in the 21st century: Same algae-different ecosystem. Journal of Great Lakes Research 36: 248-255.
4. BADGLEY, B. D., J. FERGUSON, A. Vanden Heuvel, G. T. KLEINHEINZ, C. M. McDermott, T. R. Sandrin, J. KINZELMAN, et al. 2011. Multiscale temporal and spatial variation in genotypic composition of Cladophora -borne Escherichia coli populations in Lake Michigan. Water Research 45: 721-731.
5. BAKER, G. C., J. J. SMITH, and D. A. COWAN. 2003. Review and re-analysis of domain-specific 16S primers. Journal of Microbiological Methods 55: 541-555.
6. BASTVIKEN, D., J. COLE, M. PACE, and L. TRANVIK. 2004. Methane emission from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochemical Cycles 18: GB409.
7. BASTVIKEN, D., L. J. TRANVIK, J. A. DOWNING, P. M. CRILL, and A. ENRICHPRAST. 2011. Freshwater methane emissions offset the continental carbon sink. Science 331: 50.
8. BAUTISTA, A. I. N., and O. Necchi-Júnior. 2008. Photoacclimation in a tropical population of Cladophora glomerata (L.) Kützing 1843 (Chlorophyta) from southeastern Brazil. Brazilian Journal of Biology 68: 129-136.
9. BERGEY, E. A., C. A. BOETTIGER, and V. H. RESH. 1995. Effects of water velocity on the architecture and epiphytes of Cladophora glomerata (Chlorophyta). Journal of Phycology 31: 264-271.
10. BEVERSDORF, L., S. Bornstein-Forst, and S. L. McLellan. 2007. The potential for beach sand to serve as a reservoir for Escherichia coli and the physical influences on cell die-off. Journal of Applied Microbiology 102: 1372-1381.
11. BIRCH, P. B., J. O. GABRIELSON, and K. S. HAMEL. 1983. Decomposition of Cladophora. I. Field studies in the Peel-Harvey Estuarine System, Western Australia. Botanica Marina 26: 165-171.
12. BROCK, T. D. 1985. A eutrophic lake, Lake Mendota, Wisconsin. Springer-Verlag, New York, New York, USA.
13. BURKE, C., P. STEINBERG, D. RUSCH, S. KJELLEBERG, and T. THOMAS. 2011. Bacterial community assembly based on functional genes rather than species. Proceedings of the National Academy of Sciences, USA 108: 14288-14293.
14. BYAPPANAHALLI, M. N., D. A. SHIVELY, M. B. NEVERS, M. J. SADOWSKY, and R. L. WHITMAN. 2003. Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). Federation of European Microbiological Societies, Microbial Ecology 46: 203-211.
15. CANALE, R. P., and M. T. AUER. 1982. Ecological studies and mathematical modeling of Cladophora in Lake Huron: 5. Model development and calibration. Journal of Great Lakes Research 8: 112-125.
16. CHENEY, C., and R. A. HOUGH. 1983. Factors controlling photosynthetic productivity in a population of Cladophora fracta (Chlorophyta). Ecology 64: 68-77.
17. CHOO, K.-S., P. SNOEIJS, and M. PEDERSÉN. 2002. Uptake of inorganic carbon by Cladophora glomerata (Chlorophyta) from the Baltic Sea. Journal of Phycology 38: 493-502.
18. CLARRIDGE, J. E. 2004. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clinical Microbiology Reviews 17: 840-862.
19. 12 through a symbiotic relationship with bacteria. Nature 438: 90-93.
20. CROFT, M. T., M. J. WARREN, and A. G. SMITH. 2006. Algae need their vitamins. Eukaryotic Cell 5: 1175-1183.
21. DALIGAULT, H., A. LAPIDA, A. ZEYTUN, M. NOLAN, S. LUCAS, T. G. DEL RIO, H. TICE, ET AL. 2011. Complete genome sequence of Haliscomenobacter hydrossis type strain (O T). Standards in Genomic Sciences 4: 352-360.
22. de Menezes, A. B., R. J. LOCKHARD, M. J. COX, H. E. ALLISON, and A. J. McCarthy. 2008. Cellulose degradation by micromonosporas recovered from freshwater lakes and classification of the actinomycetes by DNA gyrase B gene sequencing. Applied and Environmental Microbiology 74: 7080-7084.
23. DODDS, W. K., and D. A. GUDDER. 1992. The ecology of Cladophora. Journal of Phycology 28: 415-427.
24. DONDERSKI, W. 1991. Production of B-vitamins by heterotrophic planktonic bacteria isolated from pelagic zone of the Lake Jeziorak. Journal of the Islamic Academy of Science 4: 54-57.
25. ENGLEBERT, E. T., C. McDermott, and G. T. KLEINHEINZ. 2008a. Effects of the nuisance algae, Cladophora, on Escherichia coli at recreational beaches in Wisconsin. Science of the Total Environment 404: 10-17.
26. ENGLEBERT, E. T., C. McDermott, and G. T. KLEINHEINZ. 2008b. Impact of the alga Cladophora on the survival of E. coli, Salmonella, and Shigella in laboratory microcosm. Journal of Great Lakes Research 34: 377-382.
27. ENSMINGER, I., C. HAGEN, and W. BRAUNE. 2000a. Strategies providing success in a variable habitat: I. Relationships of environmental factors and dominance of Cladophora glomerata. Plant, Cell & Environment 23: 1119-1128.
28. ENSMINGER, I., C. HAGEN, and W. BRAUNE. 2000b. Strategies providing success in a variable habitat: Ecophysiology of photosynthesis of Cladophora glomerata. Plant, Cell & Environment 23: 1129-1136.
29. FISHER, M. W., L. W. WILCOX, and L. E. GRAHAM. 1998. Molecular characterization of epiphytic bacterial communities on charophycean green algae. Applied and Environmental Microbiology 64: 4384-4389.
30. FLEMING, E. J., A. E. LANGDON, M. Martinez-Garcia, R. STEPANAUSKAS, N. J. POULTON, E. D. P. Masland, and D. EMERSON. 2011. What's new is old: Resolving the identity of Leptothrix ochracea using single cell genomics, pyrosequencing and FISH. Public Library of Science One 6: e17769. doi:10.1371/journal.pone.0017769
31. GERLOFF, G. C., and G. P. FITZGERALD. 1976. The nutrition of Great Lakes Cladophora. EPA-600/3-79-044, U. S. Environmental Protection Agency, Office of Research and Development, Environmental Research Laboratory, Duluth, Minnesota USA.
32. GRAHAM, J. M., M. T. AUER, R. P. CANALE, and J. P. HOFFMANN. 1982. Ecological studies and mathematical modeling of Cladophora in Lake Huron: 4. Photosynthesis and respirations as functions of light and temperature. Journal of Great Lakes Research 8: 100-111.
33. GRAHAM, L. E. 1982. Cytology, ultrastructure, taxonomy, and phylogenetic relationships of Great Lakes filamentous algae. Journal of Great Lakes Research 8: 3-9.
34. GRAHAM, L. E., J. M. GRAHAM, and L. W. WILCOX. 2009. Algae. Pearson, San Francisco, California, USA.
35. GUEDON, E., S. PAYOT, M. DESVAUX, and H. PETITMANGE. 1999. Carbon and electron flow in Clostridium cellulolyticum grown in chemostat culture on synthetic medium. Journal of Bacteriology 181: 3262-3269.
36. HIGGINS, S. N., S. Y. MALKIN, E. T. HOWELL, S. J. GUILDFORD, L. CAMPBELL, V. Hirart-Baer, and R. E. HECKY. 2008. An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes. Journal of Phycology 44: 839-854.
37. 12 concentration in the multicellular alga Cladophora glomerata (Chlorophyta). Limnology and Oceanography 35: 100-108.
38. HOFFMANN, J. P., and L. E. GRAHAM. 1984. Effects of selected physicochemical factors on growth and zoosporogenesis of Cladophora glomerata (Chlorophyta). Journal of Phycology 20: 1-7.
39. HOLLANTS, J., O. LEROUX, F. LELIAERT, H. DECLEYRE, O. De Clerck, and A. WILLEMS. 2011. Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). Public Library of Science One 6: e26458.
40. HOOVER, S. W., W. D. Marner II, A. K. BROWNSON, R. M. LENNEN, T. M. WITTKOPP, J. YOSHITANI, S. ZULKIFLY, et al. 2011. Bacterial production of free fatty acids from freshwater macroalgal cellulose. Applied Microbiology and Biotechnology 91: 435-446.
41. INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE. 2012. Chapter 2.10.2, Direct global warming potentials. In S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M.Tignor, and H.L. Miller [eds.], Climate Change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change [online]. Cambridge University Press, Cambridge, New York, New York, USA. Website http://www.ipcc.ch/publications_and_data/ar4/wg1/en/ch2s2-10-2.html.
42. ISHII, S., T. YAN, D. A. SHIVELY, M. N. BYAPPANAHALLI, R. L. WHITMAN, and M. J. SADOWSKY. 2006. Cladophora (Chlorophyta) spp. harbor human bacterial pathogens in nearshore water of Lake Michigan. Applied and Environmental Microbiology 72: 4545-4553.
43. JANSSON, A.-M. 1967. The food-web of the Cladophora -belt fauna. Helgoland Marine Research 15: 574-588.
44. JOHNSON, M., S. SHIVKUMAR, and L. Berlowitz-Tarrant. 1996. Structure and properties of filamentous green algae. Materials Science and Engineering B 38: 103-108.
45. JONES, C. G., J. H. LAWTON, and M. SHACHAK. 1994. Organisms as ecological engineers. Oikos 69: 373-386.
46. KRAUFVELIN, P., and S. SALOVIUS. 2004. Animal diversity in Baltic rocky shore macroalgae: Can Cladophora glomerata compensate for lost Fucus vesiculosis? Estuarine, Coastal and Shelf Science 61: 369-378.
47. KWON, D. D., Y. K. LEE, and H. K. LEE. 2006. Costertonia aggregate gen. nov., sp. nov., a mesophilic marine bacterium of the family Flavobacteriaceae, isolated from a mature biofilm. International Journal of Systematic and Evolutionary Microbiology 56: 1349-1353.
48. LACHNIT, T., D. MESKE, M. WAHL, T. HARDER, and R. SCHMITZ. 2011. Epibacterial community patterns on marine macroalgae are hostspecific but temporally variable. Environmental Microbiology 13: 655-665.
49. LEE, K.-C., R. I. WEBB, and J. A. FUERST. 2009a. The cell cycle of the planctomycete Gemmata obscuriglobus with respect to cell compartmentalization. BMC Cell Biology 10: 4.
50. LEE, K.-C., R. I. WEBB, P. H. JANSSEN, P. SANGWAN, T. ROMEO, J. T. STALEY, and J. A. FUERST. 2009b. Phylum Verrucomicrobia representatives share a compartmented cell plan with members of bacterial phylum Planctomycetes. BMC Microbiology 9: 5.
51. LOWE, R. L., B. H. ROSEN, and J. C. KINGSTON. 1982. A comparison of epiphytes on Bangia atropurpurea (Rhodophyta) and Cladophora glomerata (Chlorophyta) from northern Lake Michigan. Journal of Great Lakes Research 8: 164-168.
52. MALKIN, S. Y., R. J. SORICHETTI, J. A. Wiklund., and R. E. Hecky. 2009. Seasonal abundance, community composition, and silica content of diatoms epiphytic on Cladophora glomerata. Journal of Great Lakes Research 35: 199-205.
53. MARSHALL, K., I. JOINT, M. E. CALLOW, and J. A. CALLOW. 2006. Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza. Microbial Ecology 52: 302-310.
54. MATSUO, Y., H. IMAGAWA, M. NISHIZAWA, and Y. SHIZURI. 2005. Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307: 1598.
55. McDonald, J. E., A. B. de Menezes, H. E. ALLISON, and A. J. McCarthy. 2009. Molecular biological detection and quantification of novel Fibrobacter populations in freshwater lakes. Applied and Environmental Microbiology 75: 5148-5152.
56. MEDIE, F. M., G. J. DAVIES, M. DRANCOURT, and B. HENRISSAT. 2012. Genome analyses highlight the different biological roles of cellulases. Nature Reviews, Microbiology 10: 227-234.
57. METZKER, M. L. 2010. Sequencing technologies-The next generation. Nature Reviews, Genetics 11: 31-46.
58. MIHRANYAN, A. 2011. Cellulose from cladophorales green algae: From environmental problem to high-tech composite materials. Journal of Applied Polymer Science 119: 2449-2460.
59. MPAWENAYO, B., and J. M. MATHOOKO. 2005. The structure of diatom assemblages associated with Cladophora and sediments in a highland stream in Kenya. Hydrobiologia 544: 55-67.
60. NAKANISHI, K., M. NISHIJIMA, M. NISHIMURA, K. KUWANO, and N. SAGA. 1996. Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. Journal of Phycology 32: 479-482.
61. OLAPADE, O. A., M. M. DEPAS, E. T. JENSEN, and S. L. McLellan. 2006. Microbial communities and fecal indicator bacteria associated with Cladophora mats on beach sites along Lake Michigan shores. Applied and Environmental Microbiology 72: 1932-1938.
62. PAALME, T., H. KUKK, J. KOTTA, and H. ORAV. 2002. 'In vivo' and 'in situ' decomposition of nuisance macroalgae Cladophora glomerata and Pilayella littoralis. Hydrobiologia 475/476: 469-476.
63. PATRICK, R., C. F. RHYNE, R. W. Richardson III, R. A. LARSON, T. T. BOTT, and K. ROGENMUSER. 1983. The potential for biological controls of Cladophora glomerata. EPA publication 600/3-83-065, U. S. Environmental Protection Agency, Washington, D.C., USA.
64. PAVER, S. F., and A. D. KENT. 2010. Temporal patterns in glycolate-utilizing bacterial community composition correlate with phytoplankton population dynamics in humic lakes. Microbial Ecology 60: 406-418.
65. PROVASOLI, L., and I. J. PINTNER. 1980. Bacteria induced polymorphism in an axenic laboratory strain of Ulva lactuca (Chlorophyceae). Journal of Phycology 16: 196-201.
66. RAGON, M., G. RESTAUX, D. MOREIRA, A. P. MØLLER, and P. López-Garcia. 2011. Sunlight-exposed biofilm microbial communities are naturally resistant to Chernobyl ionizing-radiation levels. Public Library of Science One 6: e21764.
67. RIVAS, R., E. VELÁZQUEZ, A. WILLEMS, N. VISCAÍNO, N. S. Subba-Rao, P. F. MATEOS, M. GILLIS, ET AL. 2002. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Applied and Environmental Microbiology 68: 5217-5222.
68. SALINERO, K. K., K. KELLER, W. S. FEIL, H. FEIL, S. TRONG, G. DIBARTOLO, and A. LAPIDUS. 2009. Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: Indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics 10: 351.
69. SCHLOSS, P. D., D. GEVERS, and S. L. WESTCOTT. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNAbased studies. Public Library of Science One 6: e273710.
70. SHEATH, R. G., and M. O. MORISON. 1982. Epiphytes on Cladophora glomerata in the Great Lakes and St. Lawrence seaway with particular reference to the red alga Chroodactylon ramosum (= Asterocytis smargdina). Journal of Phycology 18: 385-391.
71. STEVENSON, R. J., and E. F. STOERMER. 1982. Abundance patterns of diatoms on Cladophora in Lake Huron with respect to a point source of wastewater treatment plant effluent. Journal of Great Lakes Research 8: 184-195.
72. STOCK, I., and B. WIEDEMANN. 2001. Natural antimicrobial susceptibilities of Plesiomonas shigelloides strains. Journal of Antimicrobial Chemotherapy 48: 803-811.
73. SUEN, G., P. J. WEIMER, D. M. STEVENSON, F. O. AYLWARD, J. BOYUM, J. DENEKE, C. DRINKWATER, et al. 2011. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. Public Library of Science ONE 6: e18814.
74. 12-producing bacteria in the water and sediment of a carp culture pond. Aquaculture 119: 425-431.
75. 12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92: 267-276.
76. 12 auxotrophs. Proceedings of the National Academy of Sciences, USA 107: 20756-20761.
77. TATEWAKI, M., L. PROVASOLI, and I. J. PINTNER. 1983. Morphogenesis of Monostroma oxyspermum (Kütz.) Doty (Chlorophyceae) in axenic culture, especially in bialgal culture. Journal of Phycology 19: 409-416.
78. TUJULA, N. A., G. R. CROCETTI, C. BURKE, T. THOMAS, and C. HOLMSTRÖM. 2010. Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME Journal 4: 301-311.
79. van BERKUM, P., and B. D. EARDLY. 2002. The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Applied and Environmental Microbiology 68: 1132-1136.
80. VOGET, S., H. L. STEELE, and W. R. STREIT. 2006. Characterization of a metagenome-derived halotolerant cellulase. Journal of Biotechnology 126: 26-36.
81. WANG, Q., G. M. GARRITY, J. M. TIEDJE, and J. R. COLE. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261-5267.
82. WANG, Y., and P. Y. QIAN. 2009. Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. Public Library of Science ONE 4: e7401.
83. WARD, J. M., and A. RICCIARDI. 2010. Community-level effects of cooccurring native and exotic ecosystem engineers. Freshwater Biology 55: 1803-1817.
84. WHITMAN, R. L., D. A. SHIVELY, H. PAWLIK, M. B. NEVERS, and M. N. BYAPPANAHALLI. 2003. Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Applied and Environmental Microbiology 69: 4714-4719.
85. WHITTON, B. A. 1970. Biology of Cladophora in freshwaters. Water Research 4: 457-476.
86. WHITTON, B. A. 2002. Phylum Cyanophyta (Cyanobacteria). In D. M. John, B. A. Whitton, and A. J. Brook [eds.], The freshwater algal flora of the British Isles: An identification guide to freshwater and terrestrial algae, 25-122. Cambridge University Press, Cambridge, UK.
87. WOMMACK, K. E., J. BHAVSAR, and J. RAVEL. 2008. Metagenomics: Read length matters. Applied and Environmental Microbiology 74: 1453-1463.
88. YOON, J.-H., S.-J. KANG, S. PARK, and T.-K. OH. 2007. Devosia insulae sp. nov., isolated from soil, and emended description of the genus Devosia. International Journal of Systematic and Evolutionary Microbiology 57: 1310-1314.
89. YOUNG, E. B., R. C. TUCKER, and L. PANSCH. 2010. Alkaline phosphatase in freshwater Cladophora -epiphyte assemblages: Regulation in response to phosphorus supply and localization. Journal of Phycology 46: 93-101.
90. ZEHMS, T. T., C. McDermott, and G. T. KLEINHEINZ. 2008. Microbial concentrations in sand and their effect on beach water in Door County, Wisconsin. Journal of Great Lakes Research 34: 524-534.
91. ZHANG, G., G. ZENG, X. CAI, S. DENG, H. LUO, and G. SUN. 2007. Brachybacterium zhongshanense sp. nov., a cellulose-decomposing bacterium from sediment along the Qijiang River, Zhongshan City, China. International Journal of Systematic and Evolutionary Microbiology 57: 2519-2524.
92. ZHANG, H., Y. SEKIGUCHI, S. HANADA, P. HUGENHOLTZ, H. KIM, Y. KAMAGATA, and K. NAKAMURA. 2003. Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. International Journal of Systematic and Evolutionary Microbiology 53: 1155-1163.
93. ZULKIFLY, S. 2012. Seasonal dynamics of chemical and microbial components of Cladophora -dominated freshwater periphyton communities. Ph.D. dissertation, University of Wisconsin, Madison, Wisconsin, USA.