Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata

FEMS Microbiology Ecology

Volumn 82, Issue 2, 2012, Pages 316-325

  Printzen, Christian ^a,b   Fernández Mendoza, Fernando ^a,b   Muggia, Lucia ^c   Berg, Gabriele ^d   Grube, Martin ^c  

^a SENCKENBERG RESEARCH INSTITUTE   (Germany)

^b BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^c UNIVERSITY OF GRAZ   (Austria)

^d GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Alphaproteobacteria; Cetraria aculeata; Climate; Diversity; Lichens

Indexed keywords

BACTERIAL DNA;

ACID SOIL; ALPINE ENVIRONMENT; BACTERIUM; CLIMATE CHANGE; GEOGRAPHICAL DISTRIBUTION; LICHEN; MICROBIAL COMMUNITY; SPECIES DIVERSITY; SYMBIOSIS;

ALPHAPROTEOBACTERIA; ANTARCTICA; ARTICLE; CLASSIFICATION; ECOSYSTEM; GENE LIBRARY; GENETICS; GERMANY; ICELAND; LICHEN (ORGANISM); METAGENOME; MICROBIOLOGY; PHYLOGENY; SPAIN; SYMBIOSIS;

ALPHAPROTEOBACTERIA; ANTARCTIC REGIONS; DNA, BACTERIAL; ECOSYSTEM; GENE LIBRARY; GERMANY; ICELAND; LICHENS; METAGENOME; PHYLOGENY; SPAIN; SYMBIOSIS;

ACETOBACTERACEAE; ALGAE; ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CETRARIA ACULEATA;

EID: 84867709582     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01358.x     Document Type: Article

References (66)

1. Altschul S, Gish W, Miller W, Myers E & Lipman D (2009) Basic local alignment search tool. J Mol Biol 215: 404-410.
2. Bano N, Ruffin S, Athens B & Hollibaugh JT (2004) Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70: 781-789.
3. Barták M, Váczi P, Hájek J & Smykla J (2007) Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans. Polar Biol 31: 47-51.
4. Bates ST, Cropsey GWG, Caporaso JG, Knight R & Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77: 1309-1314.
5. Belova SE, Pankratov TA, Detkova EN, Kaparullina EN & Dedysh SN (2009) Acidisoma tundrae gen. nov., sp. nov. and Acidisoma sibiricum sp. nov., two acidophilic, psychrotolerant members of the Alphaproteobacteria from acidic northern wetlands. Int J Syst Evol Microbiol 59: 2283-2290.
6. Blackwood CB, Oaks A & Buyer JS (2005) Phylum- and class-specific PCR primers for general microbial community analysis. Appl Environ Microbiol 71: 6193-6198.
7. Blaha J, Baloch E, Grube M (2006) High photobiont diversity in symbioses of the euryoecious lichen Lecanora rupicola (Lecanoraceae, Ascomycota). Biol J Linn Soc 88: 283-293.
8. Cardinale M, Puglia AM & Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57: 484-495.
9. Cardinale M, Vieira de Castro J, Müller H, Berg G & Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66: 63-71.
10. Cardinale M, Steinová J, Rabensteiner J, Berg G & Grube M (2012) Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 4: 23-28.
11. Casano LM, del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, del Hoyo A, Guéra A & Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13: 806-818.
12. Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R & Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12: 2998-3006.
13. Cohen A (1980) On the graphical display of the significant components in a two-way contingency table. Commun Stat Theory Methods 9: 1025-1041.
14. Cole JR, Wang Q, Cardenas E et al. (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
15. Domaschke S, Fernández-Mendoza F & Printzen C (2012) Genetic diversity of Cetraria aculeata and its photobiont. Polar Biol. DOI: 10.3402/polar.v31i0.17353.
16. Drummond AJ & Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
17. Faith D (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61: 1-10.
18. Favia G, Ricci I, Damiani C et al. (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. P Natl Acad Sci USA 104: 9047-9051.
19. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36: 533-543.
20. Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martín MP & Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20: 1208-1232.
21. Friendly M (1992) Graphical methods for categorical data. SAS User Group International Conference Proceedings, pp. 190-200. http://datavis.ca/papers/sugi/sugi17.pdf.
22. Galloway DJ & Aptroot A (1995) Bipolar lichens: a review. Cryptog Bot 5: 184-191.
23. Gilbert SF, McDonald E, Boyle N, Buttino N, Gyi L, Mai M, Prakash N & Robinson J (2010) Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos Trans R Soc Lond B Biol Sci 365: 671-678.
24. González I, Ayuso-Sacido A, Anderson A & Genilloud O (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 54: 401-415.
25. Grube M & Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23: 72-85.
26. Grube M, Cardinale M, de Castro JVJ, Mueller H & Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3: 1105-1115.
27. Helmus MR, Bland TJ, Williams CK & Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169: E68-E83.
28. Hertel H (1988) Problems in monographing Antarctic crustose lichens. Polarforschung 58: 65-76.
29. Hodkinson B & Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163-180.
30. Hodkinson BP, Gottel NR, Schadt CW & Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14: 147-161.
31. Kappen L (1993) Plant activity under snow and ice, with particular reference to lichens. Arctic 46: 297-302.
32. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP & Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
33. Kroken S & Taylor J (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103: 645-660.
34. Lawrey J & Diederich P (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106: 80-120.
35. Lieber A, Kiesel B & Babel W (2003) Microbial diversity analysis of soil by SSCP fingerprinting technique using TGGE Maxi System. Ökophysiologie des Wurzelraumes (Merbach W, Hütsch BW & Augustin J, eds), pp. 61-65. Teubner Verlag, Stuttgart.
36. Littman RA, Bourne DG & Willis BL (2010) Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol Ecol 19: 1978-1990.
37. Longton R (1988) The Biology of Polar Bryophytes and Lichens. Cambridge University Press, Cambridge.
38. Mergaert J, Verhelst A, Cnockaert MC, Tan TL & Swings J (2001) Characterization of facultative oligotrophic bacteria from polar seas by analysis of their fatty acids and 16S rDNA sequences. Syst Appl Microbiol 24: 98-107.
39. Meyer D, Zeileis A & Hornik K (2003) Visualizing independence using extended association plots. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (Hornik K, Leisch F & Zeileis A, eds), pp. 1-8. Vienna, Austria.
40. Meyer D, Zeileis A & Hornik K (2006) The strucplot framework: visualizing multi-way contingency tables with VCD. J Stat Softw 17: 1-48.
41. Nelsen MP & Gargas A (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol 177: 264-275.
42. O'Brien H, Miadlikowska J & Lutzoni F (2005) Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur J Phycol 40: 363-378.
43. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH & Wagner H (2011)vegan Community Ecology Package R package version 2.0-2 (Available from: http://CRAN.R-project.org/package=vegan)
44. Opanowicz M & Grube M (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). Lichenologist 36: 125-131.
45. Øvstedal DO & Smith RIL (2001) Lichens of Antarctica and South Georgia. Cambridge University Press, Cambridge.
46. Pannewitz S, Green T, Schlensog M, Seppelt R, Sancho L & Schroeter B (2006) Photosynthetic performance of Xanthoria mawsonii C.W. Dodge in coastal habitats, Ross Sea region, continental Antarctica. Lichenologist 38: 67-81.
47. Paradis E, Claude J & Strimmer K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289-290.
48. Pearce DA, Cockell CS, Linstrom ES & Tranvik LJ (2007) First evidence for a bipolar distribution of dominant freshwater lake bacterioplankton. Antarct Sci 19: 245-252.
49. Peksa O & Skaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20: 3936-3948.
50. Piercey-Normore MD & DePriest PT (2001) Algal switching among lichen symbioses. Am J Bot 88: 1490-1498.
51. Piercey-Normore MD (2004) Selection of algal genotypes by three species of lichen fungi in the genus Cladonia. Can J Bot 82: 947-961.
52. Printzen C (2008) Uncharted terrain: the phylogeography of arctic and boreal lichens. Plant Ecol Divers 1: 265-271.
53. Raggio J, Pintado A, Ascaso C, La Torre De R, De Los Rios A, Wierzchos J, Horneck G & Sancho LG (2011) Whole lichen thalli survive exposure to space conditions: results of lithopanspermia experiment with Aspicilia fruticulosa. Astrobiology 11: 281-292.
54. Rao C (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21: 24-43.
55. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I & Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8: 2068-2073.
56. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O & Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2: 404-416.
57. Rosenberg E, Koren O, Reshef L, Efrony R & Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5: 355-362.
58. Sancho L, Schulz F, Schroeter B & Kappen L (1999) Bryophyte and lichen flora of South Bay (Livingston Island: South Shetland Islands, Antarctica). Nova Hedwigia 68: 301-337.
59. Schroeter B & Scheidegger C (1995) Water relations in lichens at subzero temperatures - structural-changes and carbon-dioxide exchange in the lichen Umbilicaria aprina from continental Antarctica. New Phytol 131: 273-285.
60. Schroeter B, Green TGA, Pannewitz S, Schlensog M & Sancho LG (2011) Summer variability, winter dormancy: lichen activity over 3 years at Botany Bay, 77 degrees S latitude, continental Antarctica. Polar Biol 34: 13-22.
61. Silvestro D & Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol, DOI: 10.1007/s13127-011-0056-0.
62. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
63. Tamura K, Peterson D, Peterson N, Stecher G, Nei M & Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
64. Türk R & Gärtner G (2001) Biological soil crusts of the subalpine, alpine and nival areas in the Alps. Ecological Studies, Vol. 150 (Baldwin, IT, Caldwell MM, Heldmaier G, Lange OL, Mooney HA, Schulze ED, Sommer U, Belnap J & Lange OL, eds), pp. 67-73. Springer, Berlin.
65. Wornik S & Grube M (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb Ecol 59: 150-157.
66. Yahr R, Vilgalys R & Depriest PT (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol 171: 847-860.