Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica

ISME Journal

Volumn 2, Issue 5, 2008, Pages 561-570

  Fürnkranz, Michael ^a,b   Wanek, Wolfgang ^a   Richter, Andreas ^a   Abell, Guy ^b   Rasche, Frank ^b   Sessitsch, Angela ^b  

^a UNIVERSITY OF VIENNA   (Austria)

^b ARC SEIBERSDORF RESEARCH GMBH   (Austria)

Author keywords

Cyanobacteria; Epiphytes; N2 fixation; NifH; Phyllosphere; Tropical rainforest

Indexed keywords

ARTICLE; BACTERIUM; COSTA RICA; GENETICS; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT LEAF; TREE; TROPIC CLIMATE;

BACTERIA; COSTA RICA; NITROGEN FIXATION; PHYLOGENY; PLANT LEAVES; PLANTS; TREES; TROPICAL CLIMATE;

BACTERIA (MICROORGANISMS); CARLUDOVICA; COSTUS; COSTUS LAEVIS; CYANOBACTERIA; EMBRYOPHYTA; GAMMAPROTEOBACTERIA; GRIAS CAULIFLORA; NOSTOC;

EID: 43449094654     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2008.14     Document Type: Article

References (44)

1. Albino U, Saridakis DP, Ferreira MC, Hungria M, Vinuesa P, Andrade G. (2006). High diversity of diazotrophic bacteria associated with the carnivorous plant Drosera villosa var. villosa growing in oligotrophic habitats in Brazil. Plant Soil 287: 199-207.
2. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Asthana RK, Srivastava A, Kayastha AM, Nath G, Singh SP. (2006a). Antibacterial potential of gammalinolenic acid from Fischerella sp. colonizing Neem tree bark. World J Microbiol Biotechnol 22: 443-448.
4. Asthana RK, Srivastava A, Singh AP, Deepali, Singh SP, Nath G et al. (2006b). Identification of an antimicrobial entity from the cyanobacterium Fischerella sp. isolated from bark of Azadirachta indica (Neem) tree. J Appl Phycol 18: 33-39.
5. Barraquio WL, Revilla L, Ladha JK. (1997). Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil 194: 15-24.
6. Bentley BL. (1987). Nitrogen fixation by epiphylls in a tropical rainforest. Ann Missouri Bot Gard 74: 234-241.
7. Carpenter EJ. (1992). Nitrogen fixation in the epiphyllae and root nodules of trees in the lowland tropical rainforest of Costa Rica. Acta Oecologica-Int J Ecol 13: 153-160.
8. Coxson D, Mc Intyre D, Vogel J. (1992). Pulse release of sugars and polyols from canopy bryophytes in tropical montane rain forest (Guadeloupe, French West Indies). Bioptropica 24: 121-133.
9. Edwards U, Rogall T, Blockerl H, Emde M, Böttger EC. (1989). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17: 7843-7853.
10. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T et al. (2001). Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67: 5285-5293.
11. Felsenstein J. (1993). PHYLIP, phylogenetic inference package. Department of Genetics, University of Washington: Seattle.
12. Freiberg E. (1998). Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a Costa Rican premontane rain forest. Oecologia 117: 9-18.
13. Fritz-Sheridan RP, Portécop J. (1987). Nitrogen fixation on the tropical volcano, La-Soufriere (Guadeloupe). 1. A survey of nitrogen-fixation by blue-green-algal microepiphytes and lichen endophytes. Biotropica 19: 194-199.
14. Hirano SS, Upper CD. (2000). Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae - a pathogen, ice nucleus, and epiphyte. Microbiol Mol. Biol Rev 64: 624-653.
15. Holdridge LR. (1967). Life Zone Ecology. Tropical Science Center: San José.
16. Hölscher D, Köhler L, van Dijk AIJM, Bruijnzeel LA. (2004). The importance of epiphytes to total rainfall interception by a tropical montane rain forest in Costa Rica. J Hydrol 292: 308-322.
17. Hurek T, Handley LL, Reinhold-Hurek B, Piche Y. (2002). Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant-Microbe Interact 15: 233-242.
18. Jones K. (1970). Nitrogen fixation in the phyllosphere of the Douglas Fir, Pseudotsuga douglasii. Ann Bot 34: 239-244.
19. Jukes TH, Cantor CR. (1969). Evolution of protein molecules. In: Munro HN (ed). Mammalian Protein Metabolism III. Academic Press: New York, pp 21-132.
20. Knauth S, Hurek T, Brar D, Reinhold-Hurek B. (2005). Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ Microbiol 7: 1725-1733.
21. Lambais MR, Crowley DE, Cury DE, Bull RC, Rodrigues RR. (2006). Bacterial diversity in tree canopies of the Atlantic forest. Science 312: 1917.
22. Lindow SE, Brandl MT. (2003). Microbiology of the phyllosphere. App Environ Microbiol 69: 1875-1883.
23. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
24. Lugtenberg BJJ, de Weger LA, Bennett JW. (1991). Microbial stimulation of plant growth and protection from disease. Curr Opin Biotechnol 2: 457-464.
25. Maidak BL, Cole JR, Parker CT, Garrity GM, Larsen N, Li B et al. (1999). A new version of the RDP (Ribosomal Database Project). Nucleic Acids Res 27: 171-173.
26. Mu Y, Nishiguchi T, Saito A, Isawa T, Mitsui H, Minamisawa K. (2005). Expression of the nifH gene of a Herbaspirillum endophyte in wild rice species: daily rhythm during the light-dark cycle. Appl Environ Microbiol 71: 8183-8190.
27. Murty MG. (1984). Phyllosphere of cotton as a habitat for diazotrophic microorganisms. App Environ Microbiol 48: 713-718.
28. Muyzer G, De Waal EC. (1993). Profiling of complex microbial populations by denaturating gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
29. Papen H, Gessler A, Zumbusch E, Rennenberg H. (2002). Chemolithoautotrophic nitrifiers in the phyllosphere of a spruce ecosystem receiving high atmospheric nitrogen input. Curr Microbiol 44: 56-60.
30. 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytol 173: 154-167.
31. Rai AN, Söderbeck E, Bergman B. (2000). Cyanobacteriumplant symbioses. New Phytol 147: 449-481.
32. Rasche F, Marco-Noales E, Velvis H, van Overbeek LS, López MM, van Elsas JD et al. (2006). Structural characteristics and plant-beneficial effects of bacteria colonizing the shoots of field grown conventional and genetically modified T4-lysozyme producing potatoes. Plant Soil 289: 123-140.
33. Reiter B, Bürgmann H, Burg K, Sessitsch A. (2003). Endophytic nifH gene diversity in African sweet potato. Can J Microbiol 49: 549-555.
34. Ruinen J. (1961). The phyllosphere. I. An ecologically neglected milieu. Plant Soil 15: 81-109.
35. Ruinen J. (1975). Nitrogen fixation in the phyllosphere. In: Stewart WDP (ed.) Nitrogen Fixation by Free-living Microorganisms. Cambridge University Press: London, pp 85-100.
36. Sanger F, Nicklen S, Coulson AR. (1977). DNA Sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
37. Sengupta B, Naudi AS, Samanta RK, Pal D, Sengupta DN, Sen SP. (1981). Nitrogen fixation in the phyllosphere of tropical plants: occurrence of phyllosphere nitrogen-fixing microorganisms in eastern India and their utility for the growth and nutrition of host plants. Ann Bot 48: 705-716.
38. Soares RA, Roesch LFW, Zanatta G, de Oliveira Camargo FA, Passaglia LMP. (2006). Occurrence and distribution of nitrogen fixing bacterial community associated with oat [Avena sativa) assessed by molecular and microbiological techniques. Appl Soil Ecol 33: 221-234.
39. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB et al. (2002). Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57: 1-45.
40. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. (1991). 16 s ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
41. Wolk PC. (1973). Physiology and cytological chemistry of blue-green algae. Bacteriol Rev 37: 32-101.
42. Yang CH, Crowley DE, Bomeman J, Keen NT. (2001). Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci USA 98: 3889-3894.
43. Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR. (2004). Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol 70: 973-983.
44. Zaid A, Schüette UME, Bent SJ, Williams CJ, Forney LJ, Joyce P. (2006). Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8: 929-938.