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Biodiversity and Conservation

, Volume 24, Issue 4, pp 799–817 | Cite as

Cyanobacteria in mangrove ecosystems

  • Danillo Oliveira Alvarenga
  • Janaina Rigonato
  • Luis Henrique Zanini Branco
  • Marli Fátima Fiore
Review Paper

Abstract

Mangroves are subject to the effects of tides and fluctuations in environmental conditions, which may reach extreme conditions. These ecosystems are severely threatened by human activities despite their ecological importance. Although mangroves are characterized by a highly specialized but low plant diversity in comparison to most other tropical ecosystems, they support a diverse microbial community. Adapted microorganisms in soil, water, and on plant surfaces perform fundamental roles in nutrient cycling, especially nitrogen and phosphorus. Cyanobacteria contribute to carbon and nitrogen fixation and their cells act as phosphorus storages in ecosystems with extreme or oligotrophic environmental conditions such as those found in mangroves. As the high plant productivity in mangroves is only possible due to interactions with microorganisms, cyanobacteria may contribute to these ecosystems by providing fixed nitrogen, carbon, and herbivory-defense molecules, xenobiotic biosorption and bioremediation, and secreting plant growth-promoting substances. In addition to water, cyanobacterial colonies have been detected on sediments, rocks, decaying wood, underground and aerial roots, trunks, and leaves. Some mangrove cyanobacteria were also found in association to algae or seagrasses. Few studies on mangrove cyanobacteria are available, but together they have reported a substantial number of species in these ecosystems. However, the cyanobacterial diversity in this biome has been traditionally underestimated. Though mangrove communities generally host cyanobacterial taxa commonly found in marine environments, unique microhabitats found in mangroves potentially harbor several undescribed cyanobacterial taxa. The relevance of cyanobacteria for mangrove conservation is highlighted in their use for the recovery of degraded mangroves as biostimulants or in bioremediation.

Keywords

Cyanobacteria Recovery of degraded mangroves Nitrogen Salinity 

Notes

Acknowledgments

We thank the São Paulo Research Foundation (FAPESP/BIOTA 2004/13910-6) for mangrove research support. D.O.A. was supported by FAPESP and National Council for Scientific and Technological Development (CNPq) graduate fellowships (Grants 2008/52556-4 and 132494/2010-8, respectively). J.R. was supported by Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES) National Postdoctoral Program. M.F.F. would also like to thank CNPq for a research fellowship (306607/2012-3).

Supplementary material

10531_2015_871_MOESM1_ESM.xls (67 kb)
Supplementary material 1 (XLS 67 kb)

References

  1. Adger WN, Hughes TP, Folke C, Carpenter SR, Rockström J (2005) Social-ecological resilience to coastal disasters. Science 309:1036–1039PubMedGoogle Scholar
  2. Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349Google Scholar
  3. Alongi DM (2008) Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuar Coast Shelf S 76:1–13Google Scholar
  4. Alongi DM (2009) Paradigm shifts in mangrove biology. In: Perillo GME, Wolanski E, Cahoon DR, Brinson MM (eds) Coastal wetlands: an integrated ecosystem approach. Elsevier, Amsterdam, pp 615–640Google Scholar
  5. Andreote FD, Jiménez DJ, Chaves D, Dias ACF, Luvizotto DM, Dini-Andreote F, Fasanella CC, Lopez MV, Baena S, Taketani RG, Melo IS (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS ONE 7:e38600PubMedCentralPubMedGoogle Scholar
  6. Banerjee A, Santra SC (2001) Phytoplankton of the rivers of Indian Sundarban mangrove estuary. Indian Biologist 33:67–71Google Scholar
  7. Bashan Y, Holguin G (2002) Plant growth-promoting bacteria: a potential tool for arid mangrove reforestation. Trees 16:159–166Google Scholar
  8. Bashan Y, Puente MW, Myrold DD, Toledo G (1998) In vitro transfer of fixed nitrogen from diazotrophic filamentous cyanobacteria to black mangrove seedlings. FEMS Microbiol Ecol 26:165–170Google Scholar
  9. Becher PG, Jütnner F (2005) Inseticidal compounds of the biofilm-forming cyanobacterium Fischerella sp. (ATCC 43239). Environ Toxicol 20:363–372PubMedGoogle Scholar
  10. Bentley BL, Carpenter EJ (1984) Direct transfer of newly-fixed nitrogen from free-living epiphyllous microorganisms to their host plant. Oecologia 63:109–113Google Scholar
  11. Bodelier PLE (2011) Toward understanding, managing, and protecting microbial ecosystems. Front Microbiol 2:80PubMedCentralPubMedGoogle Scholar
  12. Boopathi T, Balamurugan V, Gopinath S, Sundararaman M (2013) Characterization of IAA production by the mangrove cyanobacterium Phormidium sp. MI405019 and its influence on tobacco seed germination and organogenesis. J Plant Growth Regul 32:758–766Google Scholar
  13. Bouchez A, Pascault N, Chardon C, Bouvy M, Cecchi P, Lambs L, Herteman M, Fromard F, Got P, Leboulanger C (2013) Mangrove microbial diversity and the impact of trophic contamination. Mar Pollut Bull 66:39–46PubMedGoogle Scholar
  14. Branco LHZ, Silva SMF, Sant’Anna CL (1994) Stichosiphon mangle sp. nova, a new cyanophyte from mangrove environments. Arch Hydrobiol Suppl Algol Stud 72:1–7Google Scholar
  15. Branco LHZ, Sant’Anna CL, Azevedo MTP, Sormus L (1996) Cyanophyte flora from Cardoso Island mangroves, São Paulo state, Brazil. 1. Chroococcales. Arch Hydrobiol Suppl Algol Stud 80:101–113Google Scholar
  16. Branco LHZ, Sant’Anna CL, Azevedo MTP, Sormus L (1997) Cyanophyte flora from Cardoso Island mangroves, São Paulo state, Brazil. 2. Oscillatoriales. Arch Hydrobiol Suppl Algol Stud 84:39–52Google Scholar
  17. Branco LHZ, Moura AN, Silva AC, Bittencourt-Oliveira MC (2003) Biodiversidade e considerações biogeográficas das Cyanobacteria de uma área de manguezal do estado de Pernambuco, Brasil. Acta Bot Bras 17:585–596Google Scholar
  18. Cockel CS, Jones HL (2009) Advancing the case for microbial conservation. Oryx 43:520–526Google Scholar
  19. Danielsen F, Sorensen MK, Olwig MF, Selvam V, Parish F, Burgess ND, Hiraishi T, Karunagaram VM, Rasmussen MS, Hansen LB, Quarto A, Suryadiputra N (2005) The Asian tsunami: a protective role for coastal vegetation. Science 310:643PubMedGoogle Scholar
  20. Dittmar T, Lara RJ, Kattner G (2001) River or mangrove? Tracing major organic matter sources in tropical Brazilian coastal waters. Mar Chem 73:253–271Google Scholar
  21. Dor I (1984) Epiphytic blue-green algae (Cyanobacteria) of the Sinai mangal: considerations on vertical zonation and morphological adaptations. In: Por FD, Dor I (eds) Hydrobiology of the Mangal. Dr. W Junk, Hague, pp 33–54Google Scholar
  22. Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marbà N (2013) The role of coastal plant communities for climate change mitigation and adaptation. Nat Clim Change 3:961–968Google Scholar
  23. Dubey SK, Dubey J, Mehra S, Tiwari P, Bishwas AJ (2011) Potential use of cyanobacteria in bioremediation of industrial effluents. Afr J Biotechnol 10:1125–1132Google Scholar
  24. Engene N, Choi H, Esquenazi E, Rottacker EC, Ellisman MH, Dorrestein PC, Gerwick WH (2011) Underestimated biodiversity as a major explanation for the perceived rich secondary metabolite capacity of the cyanobacterial genus Lyngbya. Environ Microbiol 13:1601–1610PubMedCentralPubMedGoogle Scholar
  25. Engene N, Rottacker EC, Kaštovský J, Byrum T, Choi H, Ellisman MH, Komárek J, Gerwick WH (2012) Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int J Syst Evol Microbiol 62:1171–1178PubMedCentralPubMedGoogle Scholar
  26. Fasanella CC, Dias ACF, Rigonato J, Fiore MF, Soares FB Jr, Melo IS, Pizzirani-Kleiner AA, van Elsas JD, Andreote FD (2012) The selection exerted by oil contamination on mangrove fungal communities. Water Air Soil Pollut 223:4233–4243Google Scholar
  27. Ferrão-Filho AS, Kozlowaky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772PubMedCentralGoogle Scholar
  28. Freiberg E (1998) Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a costa rican premontane rain forest. Oecologia 17:9–18Google Scholar
  29. Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2011) Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecol Biogeogr 20:154–159Google Scholar
  30. Gomez-Garcia MR, Fazeli F, Grote A, Grossman AR, Bhaya D (2013) Role of polyphosphate in thermophilic Synechococcus sp. from microbial mats. J Bacteriol 195:3309–3319PubMedCentralPubMedGoogle Scholar
  31. Hanski I (2011) Habitat loss, the dynamics of biodiversity, and a perspective on conservation. Ambio 40:248–255PubMedCentralPubMedGoogle Scholar
  32. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographical patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506PubMedGoogle Scholar
  33. Hoffmann L, Komárek J, Kastovsky J (2005) System of cyanoprokaryotes (Cyanobacteria): state in 2004. Algol Stud 117:95–115Google Scholar
  34. Holguin G, Bashan Y (1996) Nitrogen fixation by Azospirillum brasilense Cd is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.). Soil Biol Biochem 28:1651–1660Google Scholar
  35. Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33:265–278Google Scholar
  36. Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF (2008) Resource partitioning and sympatric speciation among closely related bacterioplankton. Science 320:1081–1085PubMedGoogle Scholar
  37. Hussain MI, Khoja TM (1993) Intertidal and subtidal blue-green algal mats of open and mangrove areas in the Farasan Archipelago (Saudi Arabia), Red Sea. Bot Mar 36:377–388Google Scholar
  38. Jadoon WA, Nakai R, Naganuma T (2013) Biogeographical note on Antarctic microflorae: endemism and cosmopolitanism. Geosci Front 4:633–646Google Scholar
  39. Johnson ZI, Zinser ER, Coe A, McNulty NP, Malcolm E, Woodward S, Chrisholm SW (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–1740PubMedGoogle Scholar
  40. Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738–744Google Scholar
  41. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88Google Scholar
  42. Kannan L, Vasantha K (1992) Microphytoplankton of the Pichavaram mangals, south east coast of India: species composition and population density. Hydrobiologia 247:77–86Google Scholar
  43. Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Adv Mar Biol 40:81–251Google Scholar
  44. Komárek J (1985) Do all cyanophytes have a cosmopolitan distribution? Survey of the freshwater cyanophyte flora of Cuba. Arch Hydrobiol Suppl Algol Stud 38–39:359–386Google Scholar
  45. Komiyama A, Ong JE, Poungparn S (2008) Allometry, biomass, and productivity of mangrove: a review. Aquat Bot 89:128–137Google Scholar
  46. Kusmana C (2014) Distribution and current status of mangrove forests in Indonesia. In: Faridah-Hanum I, Latiff A, Hakeem KR, Ozturk M (eds) Mangrove ecosystems in asia. Springer, New York, pp 37–60Google Scholar
  47. Kyaruzi JJ, Kyewalyanga MS, Muruke MHS (2003) Cyanobacteria composition and impact of seasonality on their in situ nitrogen fixation rate in a mangrove ecosystem adjacent to Zanzibar town. West Indian Ocean J Mar Sci 2:35–44Google Scholar
  48. Lambert G, Steinke TD, Naidoo Y (1989) Algae associated with mangroves in southern African estuaries: cyanophyceae. S Afr J Bot 55:476–491Google Scholar
  49. Larkum AWD, Chen M, Li Y, Scliep M, Trampe E, West J, Salih A, Kühl M (2012) A novel epiphytic chlorophyll D-containing cyanobacterium isolated from a mangrove-associated red alga. J Phycol 48:1320–1327Google Scholar
  50. Lovelock CE, Grinham A, Adame MF, Penrose HM (2010) Elemental composition and productivity of cyanobacterial mats in an arid zone estuary in north western Australia. Wetl Ecol Manag 18:37–47Google Scholar
  51. Lugomela C, Bergman B (2002) Biological N2-fixation on mangrove pneumatophores: preliminary observations and perspectives. Ambio 31:612–613PubMedGoogle Scholar
  52. Lugomela C, Bergman B, Waterbury J (2001) Cyanobacterial diversity and nitrogen fixation in coastal areas around Zanzibar, Tanzania. Arch Hydrobiol Suppl Algol Stud 103:95–115Google Scholar
  53. Mani P (1992) Natural phytoplankton communities in Pichavaram mangroves. Ind J Mar Sci 21:278–280Google Scholar
  54. Mann FD, Steinke TD (1993) Biological nitrogen-fixation (acetylene reduction) associated with blue-green algal (cyanobacterial) communities in the Beachwood Mangrove Nature Reserve: II. Seasonal variation in acetylene reduction activity. S Af J Bot 59:1–8Google Scholar
  55. Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327PubMedGoogle Scholar
  56. Mollenhauer D, Bengtsson R, Lindstrøm EA (1999) Macroscopic cyanobacteria of the genus Nostoc: a neglected and endangered constituent of European inland aquatic biodiversity. Eur J Phycol 34:349–360Google Scholar
  57. Nabout JC, Rocha BS, Carneiro FM, Sant’Anna CL (2013) How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers Conserv 22:2907–2918Google Scholar
  58. Naidoo Y, Steinke TD, Mann FD, Bhatt A, Gairola S (2008) Epiphytic organisms on the pneumatophores of the mangrove Avicennia marina: occurrence and possible function. Afr J Plant Sci 1:12–15Google Scholar
  59. Nedumaran T, Thillairajasekar K, Perumal P (2008) Mangrove associated cyanobacteria at Pichavaram, Tamilnadu. Seaweed Res Utiln 30:77–85Google Scholar
  60. Neves MHB, Tribuzi D (1992) Les Cyanophycées de la mangrove de la “Ponta do Pai Vitório” de la région de Cabo Frio (RJ, Brésil). Acta Biol Leopold 14:29–52Google Scholar
  61. Nogueira NMC, Ferreira-Correia MM (2001) Cyanophyceae/cyanobacteria in red mangrove forest at Mosquitos and Coqueiros estuaries, São Luís, state of Maranhão, Brazil. Bras J Biol 61:347–356Google Scholar
  62. Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST (2010) Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr 55:2161–2169Google Scholar
  63. Paling EI, McComb AJ (1994) Cyanobacterial mats: a possible nitrogen source for arid-coast mangroves. Int J Ecol Environ Sci 20:47–54Google Scholar
  64. Pérez-Estrada CJ, León-Tejera H, Serviere-Zaragoza E (2012) Cyanobacteria and macroalgae from an arid environment mangrove on the east coast of the Baja California Peninsula. Bot Mar 55:187–196Google Scholar
  65. Phillips A, Lambert G, Granger JE, Steinke TD (1996) Vertical zonation of epiphytic algae associated with Avicennia marina (Forssk.) Vierh. pneumatophores at Beachwood Mangroves Nature Reserve, Durban, South Africa. Bot Mar 39:167–175Google Scholar
  66. Pimm SL, Raven P (2000) Extinction by numbers. Nature 403:843–845PubMedGoogle Scholar
  67. Pittman SJ, Pittman KM (2005) Short-term consequences of a benthic cyanobacterial bloom (Lyngbya majuscula Gomont) for fish and penaeid prawns in Moreton Bay (Queensland, Australia). Estuar Coast Shelf S 63:619–632Google Scholar
  68. Polidoro BA, Carpenter KE, Collins L, Duke NC, Ellison AM, Ellison JC, Farnsworth EJ, Fernando ES, Kathiresan K, Koedam NE, Livingstone SR, Miyagi T, Moore GE, Nam VN, Ong JE, Primavera JH, Salmo SG III, Sanciangco JC, Sukardjo S, Wang Y, Yong JWH (2010) The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS ONE 5:e10095PubMedCentralPubMedGoogle Scholar
  69. Polz MF, Hunt DE, Preheim SP, Weinreich DM (2006) Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Phil Trans R Soc B 361:2009–2021PubMedCentralPubMedGoogle Scholar
  70. Potts M (1979) Nitrogen fixation (acetylene reduction) associated with communities of heterocystous and non-heterocystous blue-green algae in mangrove forests of Sinai. Oecologia 39:359–373Google Scholar
  71. Potts M (1980) Blue-green algae (Cyanophyta) in marine coastal environments of the Sinai Peninsula; distribution, zonation, stratification and taxonomic diversity. Phycologia 19:60–73Google Scholar
  72. Pramanik A, Sundararaman M, Das S, Ghosh U, Mukherjee J (2011) Isolation and characterization of cyanobacteria possessing antimicrobial activity from the Sundarbans, the world’s largest tidal mangrove forest. J Phycol 47:731–743Google Scholar
  73. Raghukumar C, Vipparty V, David JJ, Chandramohan D (2001) Degradation of crude oil by marine cyanobacteria. Appl Microbiol Biotechnol 57:433–436PubMedGoogle Scholar
  74. Ramachandran S, Venugopalan VK (1987) Nitrogen fixation by bluegreen algae in Portonovo marine environments. J Mar Biol Ass India 29:337–343Google Scholar
  75. Ray R, Majumder N, Das S, Chowdhury C, Jana TK (2014) Biogeochemical cycle of nitrogen in a tropical mangrove ecosystem, east coast of India. Mar Chem. doi: 10.1016/j.marchem.2014.04.007 Google Scholar
  76. Rejmánková E, Komárek J, Komárková J (2004) Cyanobacteria—a neglected component of biodiversity: patterns of species diversity in inland marshes of northern Belize (Central America). Divers Distrib 10:189–199Google Scholar
  77. Rigonato J, Alvarenga DO, Andreote FD, Dias ACF, Melo IS, Fiore MF (2012) Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMS Microbiol Ecol 80:312–322PubMedGoogle Scholar
  78. Rigonato J, Kent AD, Alvarenga DO, Andreote FD, Beirigo RM, Vidal-Torrado R, Fiore MF (2013) Drivers of cyanobacterial diversity in mangrove soils in south-east Brazil. Environ Microbiol 15:1103–1114PubMedGoogle Scholar
  79. Ripkka R, Deruelles J, Waterbury JB, Herdman M, Stanier MY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  80. Sakthivel K, Kathiresan K (2012) Antimicrobial activities of marine cyanobacteria isolated from mangrove environment of south east coast of India. J Nat Prod 5:147–156Google Scholar
  81. Sakthivel K, Kathiresan K (2013) Cyanobacterial diversity from mangrove sediment of south east coast of India. Asian J Biodivers 4:190–203Google Scholar
  82. Sant’Anna CL (1988) Scytonemataceae (Cyanophyceae) from the state of São Paulo, southern Brazil. Nova Hedwig 46:519–539Google Scholar
  83. Santos HF, Carmo FL, Paes JES, Rosado AS, Peixoto RS (2011) Bioremediation of mangroves impacted by petroleum. Water Air Soil Poll 216:329–350Google Scholar
  84. Santra SC, Pal UC, Maity H, Bandyopadhyaya G (1988) Blue-green algae in saline habitats of West Bengal: systematic account. Biol Mem 14:81–108Google Scholar
  85. Selvakumar G, Sundararaman M (2001) Mangrove associated cyanobacterial species in Muthupet estuary. Seaweed Res Utiln 23:19–22Google Scholar
  86. Siegesmund MA, Johansen JR, Karsten U, Friedl T (2008) Coleofasciculus gen. nov. (Cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont. J Phycol 44:1572–1585Google Scholar
  87. Silambarasan G, Ramanathan T, Kathiresan K (2012) Diversity of marine cyanobacteria from three mangrove environment in Tamil Nadu Coast, south east coast of India. Curr Res J Biol Sci 4:235–238Google Scholar
  88. Silva SMF (1991) Cyanophyceae associated with mangrove trees at Inhaca Island, Mozambique. Bothalia 21:143–150Google Scholar
  89. Silva CSP, Genuário DB, Vaz MGMV, Fiore MF (2014) Phylogeny of culturable cyanobacteria from Brazilian mangroves. Syst Appl Microbiol 37:100–112PubMedGoogle Scholar
  90. Simmons TL, Coates RC, Clark BR, Engene N, González D, Esquenazi E, Dorrestein PC, Gerwick WH (2008) Biosynthetic origin of natural products isolated from marine microorganism-invertebrate assemblages. Proc Natl Acad Sci USA 105:4587–4594PubMedCentralPubMedGoogle Scholar
  91. Staley JT (1997) Biodiversity: are microbial species threatened? Curr Opin Biotechnol 8:340–345PubMedGoogle Scholar
  92. Stewart WDP (1963) Liberation of extracellular nitrogen by two nitrogen-fixing blue-green algae. Nature 200:1020–1021PubMedGoogle Scholar
  93. Sundararaman M, Boopathi T, Gopinath S (2007) Status of mangrove ecosystem: exploring the potential role of cyanobacteria in restoration and afforestation. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 211–224Google Scholar
  94. Thatoi H, Behera BC, Mishra RR, Dutta SK (2013) Biodiversity and biotechnology potential of microorganisms from mangrove ecosystems: a review. Ann Microbiol 63:1–19Google Scholar
  95. Thompson JR, Pacocha S, Pharino C, Klepac-Ceraj V, Hunt DE, Benoit J, Sarma-Rupavtarm R, Distel DL, Polz MF (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307:1311–1313PubMedGoogle Scholar
  96. Toledo G, Bashan Y, Soeldner A (1995a) Cyanobacteria and black mangroves in northeastern Mexico: colonization, and diurnal and seasonal nitrogen fixation on aerial roots. Can J Microbiol 41:999–1011Google Scholar
  97. Toledo G, Bashan Y, Soeldner A (1995b) In vitro colonization and increase in nitrogen-fixation of seedling roots of black mangrove inoculated by a filamentous cyanobacterium. Can J Microbiol 1:1012–1020Google Scholar
  98. Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126Google Scholar
  99. Valiela I, Bowen JL, York JK (2001) Mangrove forests: one of the world’s threatened major tropical environments. Bioscience 51:807–815Google Scholar
  100. Vyverman W, Verleyen E, Wilmotte A, Hodgson DA, Willems A, Peeters K, Vijver BV, De Wever A, Leliaert F, Sabbe K (2010) Evidence for widespread endemism among Antarctic micro-organisms. Polar Sci 4:103–113Google Scholar
  101. Williams DM (2011) Historical biogeography, microbial endemism and the role of classification: everything is endemic. In: Fontaneto D (ed) Biogeography of microscopic organisms: is everything small everywhere?. Cambrige University Press, Cambridge, pp 11–31Google Scholar
  102. Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173PubMedGoogle Scholar
  103. Zhubanova AA, Ernazarova AK, Kaiyrmanova GK, Zayadan BK, Savitskaya IS, Abdieva GZ, Kistaubaeva AS, Akimbekov NS (2013) Construction of cyanobacterial-bacterial consortium on the basis of axenic cyanobacterial cultures and heterotrophic bacteria cultures for bioremediation of oil-contaminated soils and water ponds. Russ J Plant Physiol 60:555–562Google Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Danillo Oliveira Alvarenga
    • 1
  • Janaina Rigonato
    • 1
  • Luis Henrique Zanini Branco
    • 2
  • Marli Fátima Fiore
    • 1
  1. 1.Center for Nuclear Energy in Agriculture, University of São Paulo (USP)PiracicabaBrazil
  2. 2.Institute of Bioscience, Languages and Exact SciencesSão Paulo State University (UNESP)São José do Rio PretoBrazil

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