Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome

Environmental Microbiology

Volumn 14, Issue 1, 2012, Pages 147-161

  Hodkinson, Brendan P ^a   Gottel, Neil R ^b   Schadt, Christopher W ^b,c   Lutzoni, François ^d  

^a NEW YORK BOTANICAL GARDEN   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

ARTICLE; BACTERIUM; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENE LIBRARY; GENETICS; GEOGRAPHY; LICHENS; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOTOTROPHY; PHYLOGENY; SYMBIOSIS;

BACTERIA; DNA, BACTERIAL; ECOSYSTEM; GENE LIBRARY; GEOGRAPHY; LICHENS; METAGENOME; MOLECULAR SEQUENCE DATA; PHOTOTROPHIC PROCESSES; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ACETOBACTERACEAE; ACIDOBACTERIACEAE; ALGAE; BACTERIA (MICROORGANISMS); BRUCELLACEAE; CYANOBACTERIA; FUNGI; RHIZOBIALES;

EID: 84855289236     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02560.x     Document Type: Article

References (57)

1. Adams, D.G., Bergman, B., Nierzwicki-Bauer, S.A., Rai, A.N., and Schüßler, A. (2006) Cyanobacterial-plant symbioses. In The Prokaryotes: A Handbook on the Biology of Bacteria. 3rd edn. Vol. 1: Symbiotic associations, biotechnology, applied microbiology. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds). New York, USA: Springer, pp. 331-363.
2. Arnold, A.E., Miadlikowska, J., Higgins, K.L., Sarvate, S.D., Gugger, P., Way, A., etal. (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58: 283-297.
3. Artursson, V., Finlay, R.D., and Jansson, J.K. (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8: 1-10.
4. Barns, S.M., Cain, E.C., Sommerville, L., and Kuske, C.R. (2007) Acidobactetia phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73: 3113-3116.
5. Bates, S.T., Cropsey, G.W.G., Caporaso, J.G., Walters, W.A., Knight, R., and Fierer, N. (2010) Bacterial communities of lichens: structure and potential functions. In Botany 2010. Stogran, J. (ed.). St. Louis, Missouri: Botanical Society of America, p. 1103.
6. Bates, S.T., Cropsey, G.W.G., Caporaso, J.G., Knight, R., and Fierer, N. (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77: 1309-1314.
7. Belnap, J. (2001) Factors influencing nitrogen fixation and nitrogen release in biological soil crusts. In Biological Soil Crusts: Structure, Function, and Management. Belnap, J., and Lange, O.L. (eds). New York, USA: Springer-Verlag, pp. 241-261.
8. Bray, J.R., and Curtis, J.T. (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 325-349.
9. Brodo, I.M., Sharnoff, S.D., and Sharnoff, S. (2001) Lichens of North America. New Haven, CT: Yale University Press.
10. Brosius, J., Palmer, J.L., Kennedy, J.P., and Noller, H.F. (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75: 4801-4805.
11. Cardinale, M., Puglia, A.M., and Grube, M. (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecology 57: 484-495.
12. Cardinale, M., Müller, H., Berg, G., de Castro J., and Grube, M. (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecology 66: 63-71.
13. Castro, H.F., Classen, A.T., Austin, E.E., Norby, R.J., and Schadt, C.W. (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76: 999-1007.
14. Chu, H., Fierer, N., Lauber, C.L., Caporaso, J.G., Knight, R., and Grogan, P. (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12: 2998-3006.
15. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., etal. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
16. Culberson, C.F., Culberson, W.L., and Johnson, A. (1984) Secondary compounds produced exclusively by lichens. In CRC Handbook of Microbiology 2nd edn, Vol. 5. Laskin, A.I., and Lechevalier, H.A. (eds). Boca Raton, FL: CRC Press, pp. 793-833.
17. Fierer, N., Bradford, M.A., and Jackson, R.B. (2007) Toward an ecological classification of soil bacteria. Ecology 88: 1354-1364.
18. Fierer, N., Hamady, M., Lauber, C.L., and Knight, R. (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105: 17994-17999.
19. Founoune, H., Duponnois, R., Bâ, A.M., Sall, S., Branget, I., Lorquin, J., etal. (2002) Mycorrhiza helper bacteria stimulate ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus alba. New Phytol 153: 81-89.
20. González, I., Ayuso-Sacido, A., Anderson, A., and Genilloud, O. (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecology 54: 401-415.
21. Goslee, S., and Urban, D. (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22: 1-19.
22. Grube, M., and Berg, G. (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23: 72-85.
23. Grube, M., Cardinale, M., de Castro, J.V., Jr, Muller, H., and Berg, G. (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3: 1105-1115.
24. Hamady, M., Lozupone, C., and Knight, R. (2009) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27.
25. Hodkinson, B.P., and Lutzoni, F. (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163-180.
26. Hodkinson, B.P., and Lutzoni, F. (2010) Do lichens harbor their own rhizobia? A large-scale phylogenetic survey of lichen-associated bacteria from the order Rhizobiales. Inoculum 61: 55-56.
27. Hoffman, M.T., and Arnold, A.E. (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76: 4063-4075.
28. Humbert, J.F., Dorigo, U., Cecchi, P., Berre, B.L., Debroas, D., and Bouvy, M. (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11: 2339-2350.
29. Jukes, T.H., and Cantor, C.R. (1969) Evolution of protein molecules. In Mammalian Protein Metabolism. Munro, H.N. (ed.). New York, USA: Academic Press, pp. 21-132.
30. Kuczynski, J., Liu, Z., Lozupone, C., McDonald, D., Fierer, N., and Knight, R. (2010) Microbial community resemblance methods differ in their ability to detect biologically relevant patterns. Nat Methods 7: 813-819.
31. Lawrey, J.D. (2009) Chemical defense in lichen symbiosis. In Defensive Mutualism in Microbial Symbiosis. White, J.F., and Torres, M.S. (eds). Boca Raton, FL: CRC Press, pp. 167-181.
32. Liba, C., Ferrara, F., Manfio, G., Fantinatti-Garboggini, F., Albuquerque, R., Pavan, C., etal. (2006) Nitrogen-fixing chemo- organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J Appl Microbiol 101: 1076-1086.
33. Lozupone, C., and Knight, R. (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
34. Lutzoni, F., and Pagel, M. (1997) Accelerated evolution as a consequence of transitions to mutualism. Proc Natl Acad Sci USA 94: 11422-11427.
35. Lutzoni, F., Wagner, P., Reeb, V., and Zoller, S. (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Syst Biol 49: 628-651.
36. Maddison, D., and Maddison, W. (2005) MacClade 4.08. Sunderland, MA: Sinauer Associates.
37. Moran, N.A. (1996) Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93: 2873-2878.
38. Mushegian, A.A., Peterson, C.N., Baker, C.C.M., and Pringle, A. (2011) Bacterial diversity across individual lichens. Appl Environ Microbiol 77: 4249-4252.
39. Najar-Rodríguez, A.J., McGraw, E.A., Mensah, R.K., Pittman, G.W., and Walter, G.H. (2009) The microbial flora of Aphis gossypii: patterns across host plants and geographical space. J Invertebr Pathol 100: 123-126.
40. Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Simpson, G.L., and Stevens, M.H.H. (2009) vegan: Community Ecology Package. R package version 1.15-4. [WWW document]. URL.
41. Palmqvist, K. (2002) Cyanolichens: Carbon Metabolism. In Cyanobacteria in Symbiosis. Rai, A.N., Berman, B., and Rasmussen, U. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 73-96.
42. Porter, T.M., Skillman, J.E., and Moncalvo, J.M. (2008) Fruiting body and soil rDNA sampling detects complementary assemblage of Agaricomycotina (Basidiomycota, Fungi) in a hemlock-dominated forest plot in southern Ontario. Mol Ecol 17: 3037-3050.
43. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
44. Rai, A.N. (2002) Cyanolichens: Nitrogen Metabolism. In Cyanobacteria in Symbiosis. Rai, A.N., Berman, B., and Rasmussen, U. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 97-115.
45. Riffel, A., Medina, L.F., Stefani, V., Santos, R.C., Bizani, D., and Brandelli, A. (2002) In vitro antimicrobial activity of a new series of 1, 4 naphthoquinones. Braz J Med Biol Res 35: 811-818.
46. Russell, J.A., Goldman-Huertas, B., Moreau, C.S., Baldo, L., Stahlhut, J.K., Werren, J.H., and Pierce, N.E. (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63: 624-640.
47. Rycroft, D.S., Connolly, J.D., Huneck, S., and Himmelreich, U. (1996) Revised Structure of Haemoventosin. ChemInform 27: 10.1002/chin.199610298.
48. Schaefer, A.L., Taylor, T.A., Beatty, J.T., and Greenberg, E.P. (2002) Long-Chain Acyl-Homoserine Lactone Quorum-Sensing Regulation of Rhodobacter capsulatus Gene Transfer Agent Production. J Bacteriol 184: 6515-6521.
49. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., etal. (2009) Introducing Mothur: open-source, platform- independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
50. Smit, E., Leeflang, P., Gommans, S., van den Broek, J., van Mil, S., and Wernars, K. (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.
51. Stajich, J.E., Block, D., Boulez, K., Brenner, S.E., Chervitz, S.A., Dagdigian, C., etal. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611-1618.
52. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
53. Swofford, D.L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, Mass: Sinauer Associates.
54. Taylor, M.W., Schupp, P.J., de Nys, R., Kjelleberg, S., and Steinberg, P.D. (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ Microbiol 7: 419-433.
55. Taylor, M.W., Radax, R., Steger, D., and Wagner, M. (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
56. Warnecke, F., Luginbuhl, P., Ivanova, N., Ghassemian, M., Richardson, T.H., Stege, J.T., etal. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-565.
57. Wernegreen, J.J., and Moran, N.A. (1999) Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol 16: 83-97.