The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities

Applied and Environmental Microbiology

Volumn 76, Issue 6, 2010, Pages 1851-1860

  Koopman, Margaret M ^a   Fuselier, Danielle M ^a   Hird, Sarah ^a   Carstens, Bryan C ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

454-PYROSEQUENCING; BACTERIAL COMMUNITY; BACTERIAL COMMUNITY COMPOSITION; BACTERIAL DIVERSITY; INSECT PREY; MICROBIAL COMMUNITIES; MICROBIAL DIVERSITY; PLANT LEAVES; RIBOSOMAL INTERGENIC SPACER ANALYSIS; SURROUNDING SOILS; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS; TIME POINTS; TIME-DEPENDENT;

BACTERIA;

BACTERIOLOGY;

BACTERIAL DNA; RIBOSOMAL SPACER DNA;

BACTERIUM; CARNIVOROUS PLANT; INTERSPECIFIC INTERACTION; MICROBIAL COMMUNITY; SPECIES DIVERSITY;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA FINGERPRINTING; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METAGENOME; MICROBIOLOGY; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SARRACENIACEAE; TIME;

BACTERIA; BIODIVERSITY; CLUSTER ANALYSIS; DNA FINGERPRINTING; DNA, BACTERIAL; DNA, RIBOSOMAL SPACER; METAGENOME; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SARRACENIACEAE; SEQUENCE ANALYSIS, DNA; TIME FACTORS;

BACTERIA (MICROORGANISMS); HEXAPODA; SARRACENIA; SARRACENIA ALATA; SARRACENIACEAE;

EID: 77749260566     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02440-09     Document Type: Article

References (74)

1. Addicott, J. F. 1974. Predation and prey community structure: experimental study of effect of mosquito larvae on protozoan communities of pitcher plants. Ecology 55:475-492.
2. Allen, E. B., M. F. Allen, D. J. Helm, J. M. Trappe, R. Molina, and E. Rincon. 1995. Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47-62.
3. Andrews, J. H., and R. F. Harris. 2000. The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38:145-180.
4. Andrews, J. H., C. M. Kenerley, and E. V. Nordheim. 1980. Positional variation in phylloplane populations within an apple tree canopy. Microb. Ecol. 6:71-84.
5. Bardgett, R. D., J. L. Mawdsley, S. Edwards, P. J. Hobbs, J. S. Rodwell, and W. J. Davies. 2002. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct. Ecol. 13:650-660.
6. Bardgett, R. D., and E. McAlister. 1999. The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol. Fertil. Soils 29:282-290.
7. Bent, S. J., and L. J. Forney. 2008. The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J. 2:689-695.
8. Bent, S. J., J. D. Pierson, L. J. Forney, R. Danovaro, G. M. Luna, A. Dell'Anno, and B. Pietrangeli. 2007. Measuring species richness based on microbial community fingerprints: the emperor has no clothes. Appl. Environ. Microbiol. 73:2399-2401.
9. Björk, R. G., M. P. Björkman, M. X. Andersson, and L. Klemedtsson. 2008. Temporal variation in soil microbial communities in alpine tundra. Soil Biol. Biochem. 40:266-268.
10. Bledzki, L. A., and A. M. Ellison. 2003. Diversity of rotifers from northeastern U. S. A. bogs with new species records for North America and New England. Hydrobiologia 497:53-62.
11. Blow, N. 2008. Metagenomics: exploring unseen communities. Nature 453: 687-690.
12. Bossio, D. A., K. M. Scow, N. Gunapala, and K. J. Graham. 1998. Determinants of soil microbial communities: effects of agricultural management, season and soil type on phospholipid fatty acid profiles. Microb. Ecol. 36:1-12.
13. Bradshaw, W. E. 1983. Interaction between the mosquito Wyeomyia smithii, the midge Metriocnemus knabi, and their carnivorous host Sarracenia purpurea. Plexus Publishing, Marlton, NJ.
14. Bradshaw, W. E., and R. A. Creelman. 1984. Mutualism between the carnivorous purple pitcher plant and its inhabitants. Am. Midl. Nat. 112:294-304.
15. Buckley, H. L., T. E. Miller, A. M. Ellison, and N. J. Gotelli. 2003. Reverse latitudinal trends in species richness of pitcher-plant food webs. Ecol. Lett. 6:825-829.
16. Butler, J. L., N. J. Gotelli, and A. M. Ellison. 2008. Linking the brown and green: nutrient transformation and fate in the Sarracenia microecosystem. Ecology 89:898-904.
17. Cardinale, M., L. Brusetti, P. Quatrini, S. Borin, A. M. Puglia, A. Rizzi, E. Zanardini, C. Sorlini, C. Corselli, and D. Daffonchio. 2004. Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl. Environ. Microbiol. 70:6147-6156.
18. Clarke, K. R., and M. Ainsworth. 1993. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 92:205-219.
19. Clarke, K. R., and R. N. Gorley. 2006. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth, United Kingdom.
20. Cochran-Stafira, D. L., and C. E. von Ende. 1998. Integrating bacteria into food webs: studies with Sarracenia purpurea inquilines. Ecology 79:880-898.
21. Culman, S. W., R. Bukowski, H. G. Gauch, H. Cadillo-Quiroz, and D. H. Buckley. 2009. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinform. 10:171.
22. Curtis, T. P., W. Sloan, and J. Scannell. 2002. Estimating prokaryotic diversity and its limits. Proc. Natl. Acad. Sci. U. S. A. 99:10494-10499.
23. Curtis, T. P., and W. T. Sloan. 2004. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr. Opin. Microbiol. 7:221-226.
24. Denaro, R. G., G. D'Auria, M. Di Marco, M. Genovese, M. Troussellier, M. M. Yakimov, and L. Giuliano. 2005. Assessing terminal restriction fragment length polymorphism suitability for the description of bacterial community structure and dynamics in hydrocarbon-polluted marine environments. Environ. Microbiol. 7:78-87.
25. Dunbar, J., L. O. Ticknor, and C. R. Kuske. 2001. Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl. Environ. Microbiol. 67:190-197.
26. Ercolani, G. L. 1991. Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb. Ecol. 21:35-48.
27. Fierer, N., M. Hamady, C. L. Lauber, and R. Knight. 2008. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc. Natl. Acad. Sci. U. S. A. 105:17994-17999.
28. Fish, D., and D. W. Hall. 1978. Succession and stratification of aquatic insects inhabiting leaves of the insectivorous pitcher plant, Sarracenia purpurea. Am. Midl. Nat. 99:172-183.
29. Garbeva, P., J. A. Van Veen, and J. D. Van Elsas. 2004. Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu. Rev. Phytopathol. 42:243-270.
30. Giglioli, I. 1897. Insects and yeasts. Nature 56:575-577.
31. Gilbert, D. G. 1980. Dispersal of yeasts and bacteria by Drosophila in a temperate forest. Oecologia 46:135-137.
32. Hamady, M., J. Walker, J. Harris, N. Gold, and R. Knight. 2008. Error-correcting barcoded primers allow hundreds of samples to be pyrosequenced in multiplex. Nat. Methods 5:235-237.
33. Harvey, E., and T. E. Miller. 1996. Variance in composition of inquiline communities in leaves of Sarracenia purpurea L. on multiple spatial scales. Oecologia 108:562-566.
34. Heard, S. B. 1994. Pitcher-plant midges and mosquitos: a processing chain commensalism. Ecology. 75:1647-1660.
35. Hepburn, J. S., E. Q. St. John, and F. M. Jones. 1927. The absorption of nutrients in the pitchers of the Sarraceniaceae. Trans. Wagner Free Inst. Sci. 11:85-86.
36. Hugenholtz, P., and G. W. Tyson. 2008. Microbiology: metagenomics. Nature 455:481-483.
37. Istock, C. A., S. S. Wasserman, and H. Zimmer. 1975. Ecology and evolution of pitcher-plant mosquito. 1. Population dynamics and laboratory responses to food and population density. Evolution 29:296-312.
38. Jones, S. E., A. L. Shade, K. D. McMahon, and A. D. Kent. 2007. Comparison of primer sets for use in automated ribosomal intergenic spacer analysis of aquatic bacterial communities: an ecological perspective. Appl. Environ. Microbiol. 73:659-662.
39. Kent, A. D., S. E. Jones, A. C. Yannarell, G. H. Lauster, J. H. Graham, T. K. Kratz, and E. W. Triplett. 2004. Annual patterns in bacterioplankton community variability in a humic lake. Microb. Ecol. 48:550-560.
40. Kent, A. D., D. J. Smith, B. J. Benson, and E. W. Triplett. 2003. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl. Environ. Microbiol. 69:6768-6776.
41. Kent, A. D., A. C. Yannarell, J. A. Rusak, E. W. Triplett, and K. D. McMahon. 2007. Synchrony in aquatic microbial community dynamics. Multidiscip. J. Microb. Ecol. 1:38-47.
42. Kinkel, L. L., M. Wilson, and S. E. Lindow. 1996. Utility of microcosm studies for predicting phylloplane bacterium population sizes in the field. Appl. Environ. Microbiol. 62:3413-3423.
43. Kneitel, J. M., and T. E. Miller. 2003. Dispersal rates affect community composition in metacommunities of Sarracenia purpurea inquilines. Am. Nat. 162:165-171.
44. Kneitel, J. M., and T. E. Miller. 2002. Resource and top-predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology 83:680-688.
45. Lambais, M. R., D. E. Crowley, J. C. Cury, R. C. Bull, and R. R. Rodrigues. 2006. Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917.
46. Lindow, S. E., and M. T. Brandl. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875-1883.
47. Lindquist, J. A. 1975. Bacteriological and ecological observations on the northern pitcher plant, Sarracenia purpurea L. M.S. thesis. University of Wisconsin - Madison.
48. Lipson, D. A., C. W. Schadt, and S. K. Schmidt. 2002. Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microb. Ecol. 43:307-314.
49. Liu, W. T., T. L. Marsh, H. Cheng, and L. J. Forney. 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.
50. Liu, Z., C. Lozupone, M. Hamady, F. D. Bushman, and R. Knight. 2007. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res. 35:e120.
51. Maguire, B., Jr. 1963. The passive dispersal of small aquatic organisms and their colonization of isolated bodies of water. Ecol. Monogr. 33:161-185.
52. Margulies, M., et al. 2005. Genome sequencing in microfabricated highdensity picolitre reactors. Nature 437:376-380.
53. McPherson, S. 2007. Pitcher plants of the Americas. The McDonald and Woodward Publishing Company, Blacksburg, VA.
54. Miller, T. E., D. Cassill, C. Johnson, C. Kindell, J. Leips, D. McInnes, T. Bevis, D. Mehlman, and B. Richard. 1994. Intraspecific and interspecific competition of Wyeomyia smithii (Coq) (Culicidae) in pitcher plant communities. Am. Midl. Nat. 131:136-145.
55. Miller, T. E., and J. M. Kneitel. 2002. Inquiline communities in pitcher plants as a prototypical metacommunity. University of Chicago Press, Chicago, IL.
56. Miller, T. E., J. M. Kneitel, and J. H. Burns. 2002. Effect of community structure on invasion success and rate. Ecology 83:898-905.
57. Myers, R. T., D. R. Zaka, D. C. White, and A. Peacock. 2001. Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci. Soc. Am. J. 65:359-367.
58. O'Brien, R. D., and S. E. Lindow. 1989. Effect of plant species and environmental conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathology 69:619-627.
59. Peterson, C. N., S. Day, B. E. Wolfe, A. M. Ellison, R. Kolter, and A. Pringle. 2008. A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environ. Microbiol. 10:2257-2266.
60. Plummer, G. L., and T. H. Jackson. 1963. Bacterial activities within the sarcophagus of the insectivorous plant, Sarracenia flava. Am. Midl. Nat. 69:462-469.
61. Prankevicius, A. B., and D. M. Cameron. 1991. Bacterial dinitrogen fixation in the leaf of the northern pitcher plant (Sarracenia purpurea). Can. J. Bot. 69:2296-2298.
62. Redford, A. J., and N. Fierer. 2009. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb. Ecol. 58:189-198.
63. Revill, D. L., K. W. Stewart, and J. H. E. Schlichting. 1967. Passive dispersal of viable algae and protozoa by certain craneflies and midges. Ecology 49:1023-1027.
64. Reynolds, H. L., A. Packer, J. D. Bever, and K. Clay. 2003. Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 48:2281-2291.
65. Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10.
66. Schweitzer, J. A., J. K. Bailey, R. K. Bangert, S. C. Hart, and T. G. Whitham. 2006. Above- and below-ground microbial communities. CABI, Cambridge, MA.
67. Siragusa, A. J., J. E. Swenson, and D. A. Casamatta. 2007. Culturable bacteria present in the fluid of the hooded-pitcher plant Sarracenia minor based on 16S rDNA gene sequence data. Microb. Ecol. 54:324-331.
68. Smit, E., P. Leeflang, S. Gommans, J. van den Broek, S. van Mil, and K. Wernars. 2001. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl. Environ. Microbiol. 67:2284-2291.
69. Thompson, I. P., M. J. Bailey, J. S. Fenlon, T. R. Fermor, A. K. Lilley, J. M. Lynch, P. J. McCormack, M. P. McQuilken, K. J. Purdy, P. B. Rainey, and J. M. Whipps. 1993. Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris). Plant Soil 150:177-191.
70. van der Gast, C. J., D. Ager, and A. K. Lilley. 2008. Temporal scaling of bacterial taxa is influenced by both stochastic and deterministic ecological factors. Environ. Microbiol. 10:1411-1418.
71. Waldrop, M. P., and M. K. Firestone. 2006. Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb. Ecol. 52:470-479.
72. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
73. Wilson, M., and S. E. Lindow. 1994. Inoculum density-dependent mortality and colonization of the phyllosphere by Pseudomonas syringae. Appl. Environ. Microbiol. 60:2232-2237.
74. Yannarell, A. C., and E. W. Triplett. 2005. Geographic and environmental sources of variation in lake bacterial community composition. Appl. Environ. Microbiol. 71:227-239.