Abstract
The diversity and physiological characteristics of culturable bacteria associated with lichens from different habitats of the Arctic and Antarctica were investigated. The 68 retrieved isolates could be grouped on the basis of their 16S rRNA gene sequences into 26 phylotypes affiliated with the phyla Actinobacteria, Bacteroidetes, Deinococcus-Thermus, and Firmicutes and with the classes Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria. Isolates belonging to the Alphaproteobacteria were the most abundant, followed by those belonging to Actinobacteria, Betaproteobacteria, Gammaproteobacteria, Bacteroidetes, Firmicutes, and Deinococcus-Thermus. Phylogenetic analysis showed that approximately 21 % of the total isolates represented a potentially novel species or genus (≤97 % sequence similarity). Strains belonging to the genera Sphingomonas, Frondihabitans, Hymenobacter, and Burkholderia were recovered from lichen samples from both geographic locations, implying common and important bacterial functions within lichens. Extracellular protease activities were detected in six isolates, affiliated with Burkholderia, Frondihabitans, Hymenobacter, Pseudomonas, and Rhodanobacter. Extracellular lipase activities were detected in 37 isolates of the genera Burkholderia, Deinococcus, Frondihabitans, Pseudomonas, Rhodanobacter, Sphingomonas, and Subtercola. This is the first report on the culturable bacterial diversity present within lichens from Arctic and Antarctica and the isolates described herein are valuable resources to decode the functional and ecological roles of bacteria within lichens. In addition, the low similarity (≤97 %) of the recovered isolates to known species and their production of cold-active enzymes together suggest that lichens are noteworthy sources of novel bacterial strains for use in biotechnological applications.
Similar content being viewed by others
References
Asker D, Beppu T, Ueda K (2007) Sphingomonas astaxanthinifaciens sp. nov., a novel astaxanthin-producing bacterium of the family Sphingomonadaceae isolated from Misasa, Tottori, Japan. FEMS Microbiol Lett 273:140–148
Balandreau J, Viallard V, Cournoyer B, Coenye T, Laevens S, Vandamme P (2001) Burkholderia cepacia genomovar III is a common plant-associated bacterium. Appl Environ Microbiol 67:982–985
Bates ST, Cropsey GWG, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314
Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495
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
Copley SD (2000) Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem Sci 25:261–265
Ederer MM, Crawford RL, Herwig RP, Orser CS (1997) PCP degradation is mediated by closely related strains of the genus Sphingomonas. Mol Ecol 6:39–49
Estrada-De Los Santos P, Bustillos-Cristales RO, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798
Fujii M, Takano Y, Kojima H, Hoshino T, Tanak R, Fukui M (2010) Microbial community structure, pigment composition, and nitrogen source of red snow in Antarctica. Microb Ecol 59:466–475
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
Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85
Hodkinson B, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180
Kappen L (2000) Some aspects of the great success of lichens in Antarctica. Antarctic Sci 12:314–324
Kim H, Nishiyama M, Kunito T, Senoo K, Kawahara K, Murakami K, Oyaizu H (1998) High population of Sphingomonas species on plant surface. J Appl Microbiol 85:731–736
Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic Acid Techniques in Bacterial Systematics. Wiley, New York, pp 115–175
Lee Y, Kim G, Jung Y-J, Choe C-D, Yim J, Lee H, Hong S (2012) Polar and alpine microbial collection (PAMC): a culture collection dedicated to polar and alpine microorganisms. Polar Biol 35:1433–1438
Liba CM, Ferrara FIS, Manfio GP, Fantinatti-Garboggini F, Albuquerque RC, Pavan C, Ramos PL, Moreira-Filho CA, Barbosa HR (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
Peeters K, Ertz D, Willems A (2011) Culturable bacterial diversity at the Princess Elisabeth Station (Utsteinen, Sør Rondane Mountains, East Antarctica) harbours many new taxa. Syst Appl Microbiol 34:360–367
Printzen C, Fernández-Mendoza F, Muggia L, Berg G, Grube M (2012) Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol Ecol 82:316–325
Reis VM, Santos PE-d, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Selbmann L, Zucconi L, Ruisi S, Grube M, Cardinale M, Onofri S (2010) Culturable bacteria associated with antarctic lichens: affiliation and psychrotolerance. Polar Biol 33:71–83
Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. Nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192
Sheng HM, Gao HS, Xue LG, Ding S, Song CL, Feng HY, An LZ (2011) Analysis of the composition and characteristics of culturable endophytic bacteria within subnival plants of the Tianshan mountains, Northwestern China. Curr Microbiol 62:923–932
Singh OV, Gabani P (2011) Extremophiles: radiation resistance microbial reserves and therapeutic implications. J Appl Microbiol 110:851–861
Videira SS, De Araujo JLS, Da Silva Rodrigues L, Baldani VLD, Baldani JI (2009) Occurrence and diversity of nitrogen-fixing Sphingomonas bacteria associated with rice plants grown in Brazil. FEMS Microbiol Lett 293:11–19
Wang Y, Dai C–C (2011) Endophytes: a potential resource for biosynthesis, biotransformation, and biodegradation. Ann Microbiol 61:207–221
Acknowledgments
This research was supported by the Korea Polar Research Institute (Grants PE11050, PE14020, and PE14080).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lee, Y.M., Kim, E.H., Lee, H.K. et al. Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria. World J Microbiol Biotechnol 30, 2711–2721 (2014). https://doi.org/10.1007/s11274-014-1695-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-014-1695-z