Novel bacteria associated with Arctic seashore lichens have potential roles in nutrient scavenging

Canadian Journal of Microbiology

Volumn 60, Issue 5, 2014, Pages 307-317

  Sigurbjörnsdóttir, Margrét Audur ^a   Heidmarsson, Starri ^b   Jónsdóttir, Anna Rut ^a   Vilhelmsson, Oddur ^a  

^a UNIVERSITY OF AKUREYRI   (Iceland)

^b ICELANDIC INSTITUTE OF NATURAL HISTORY   (Iceland)

Author keywords

Bacterial community; Biodegradation; Lichens; Saxicolous; Symbiosis

Indexed keywords

BETA GLUCAN; BIOPOLYMER; CHITOSAN; DNA 16S; LIGNIN; PHOSPHATE; XYLAN;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ARCTIC; ARTICLE; BACILLI; BACTERIAL FLORA; BACTERIAL STRAIN; BACTERIUM; BACTERIUM ISOLATE; BIODEGRADATION; CELL PHAGOCYTOSIS; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; FLAVOBACTERIA; GAMMAPROTEOBACTERIA; HALOPHILIC BACTERIUM; ICELAND; LICHEN (ORGANISM); MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; PHYLOGENY; PRIORITY JOURNAL; SCAVENGING SYSTEM; SEASHORE; SPHINGOBACTERIA;

BACTERIAL COMMUNITY; BIODEGRADATION; BIODÉGRADATION; COMMUNAUTÉ BACTÉRIENNE; LICHENS; SAXICOLE; SAXICOLOUS; SYMBIOSE; SYMBIOSIS;

ARCTIC REGIONS; BACTERIA; ICELAND; LICHENS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84899785059     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2013-0888     Document Type: Article

References (59)

1. Adachi, M., Kanno, T., Okamoto, R., Shinozaki, A., Fujikawa-Adachi, K., and Nishijima, T. 2004. Jannaschia cystaugens sp. nov., an Alexandrium (Dinophyceae) cyst formation-promoting bacterium from Hiroshima Bay, Japan. Int. J. Syst. Evol. Microbiol. 54: 1687-1692. doi:10.1099/ijs.0.03029-0. PMID:15388729.
2. Ahmadjian, V. 1995. Lichens are more important than you think. BioScience, 45: 123-124. doi:10.1093/bioscience/45.3.124.
3. Alain, K., Intertaglia, L., Catala, P., and Lebaron, P. 2008. Eudoraea adriatica gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 58: 2275-2281. doi:10.1099/ijs.0.65446-0. PMID:18842840
4. Baldursdóttir, S. 1985. Marine og maritime likener på nogle klippekyster i Island. M.Sc. thesis, Institut for Sporeplanter, Københavns Universitet, Copenhagen, Denmark.
5. Banfield, J.F., Barker, W.W., Welch, S.A., and Taunton, A. 1999. Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc. Natl. Acad. Sci. U.S.A. 96: 3404-3411. doi:10.1073/pnas.96.7.3404. PMID:10097050.
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. doi:10.1128/AEM.02257-10. PMID:21169444.
7. Bjelland, T., Grube, M., Hoem, S., Jorgensen, S.L., Daae, F.L., Thorseth, I.H., and Øvreås, L. 2011. Microbial metacommunities in the lichen-rock habitat. Environ. Microbiol. Reports, 3(4): 434-442. doi:10.1111/j.1758-2229.2010.00206.x. PMID:23761305.
8. Bowman, J.P., McCammon, S.A., Brown, M.V., Nichols, D.S., and McMeekin, T.A. 1997. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl. Environ. Microbiol. 63: 3068-3078. PMID:9251193.
9. Brümmer, I.H.M., Fehr, W., and Wagner-Döbler, I. 2000. Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl. Environ. Microbiol. 66: 3078-3082. doi: 10.1128/AEM.66.7.3078-3082.2000. PMID:10877809.
10. Buczolits, S., Denner, E.B.M., Vybrial, D., Wieser, M., Kämpfer, P., and Busse, H.J. 2002. Classification of three airborne bacteria and proposal of Hymenobacter aerophilus sp. nov. Int. J. Syst. Evol. Microbiol. 52(2): 445-456. doi:10.1099/ijs. 0.01682-0. PMID:11931156.
11. Cardinale, M., Puglia, A.M., and Grube, M. 2006. Molecular analysis of lichenassociated bacterial communities. FEMS Microbiol. Ecol. 57(3): 484-495. doi: 10.1111/j.1574-6941.2006.00133.x. PMID:16907761.
12. Cardinale, M., de Castro, J.V., Müller, H., Berg, G., and 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(1): 63-71. doi:10.1111/j.1574-6941.2008.00546.x. PMID:18631179.
13. Cavicchioli, R., Fegatella, F., Ostrowski, M., Eguchi, M., and Gottschal, J. 1999. Sphingomonads from marine environments. J. Ind. Microbiol. Biotechnol. 23(4-5): 268-272. doi:10.1038/sj.jim.2900732. PMID:11423943.
14. Cavicchioli, R., Ostrowski, M., Fegatella, F., Goodchild, A., and Guixa-Boixereu, N. 2003. Life under nutrient limitation in oligotrophic marine environments: an eco/physiological perspective of Sphingopyxis alaskensis (formerly Sphingomonas alaskensis). Microb. Ecol. 45(3): 203-217. doi:10.1007/ s00248-002-3008-6. PMID:12632213.
15. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37: D141-D145. doi:10.1093/nar/gkn879. PMID: 19004872.
16. Collins, M.D., Hutson, R.A., Grant, I.R., and Patterson, M.F. 2000. Phylogenetic characterization of a novel radiation-resistant bacterium from irradiated pork: description of Hymenobacter actinosclerus sp. nov. Int. J. Syst. Evol. Microbiol. 50(2): 731-734. doi:10.1099/00207713-50-2-731. PMID:10758882.
17. de los Ríos, A., Wierzchos, J., and Ascaso, C. 2002. Microhabitats and chemical microenvironments under saxicolous lichens growing on granite. Microb. Ecol. 43(1): 181-188. doi:10.1007/s00248-001-1028-2. PMID:11984640.
18. Fredrickson, J.K., Balkwill, D.L., Romine, M.F., and Shi, T. 1999. Ecology, physiology, and phylogeny of deep subsurface Sphingomonas sp. J. Ind. Microbiol. Biotechnol. 23: 273-283. doi:10.1038/sj.jim.2900741. PMID:11423944.
19. Gadd, G.M. 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 111: 3-49. doi:10.1016/j.mycres.2006.12.001. PMID:17307120.
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. Ecol. 54(3): 401-415. doi:10. 1016/j.femsec.2005.05.004. PMID:16332338.
21. Grube, M., Cardinale, M., de Castro, J.V., Jr., Müller, H., and Berg, G. 2009. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J. 3: 1105-1115. doi:10.1038/ismej.2009.63. PMID: 19554038.
22. Grube, M., Berg, G., Andrésson, Ó.S., Vilhelmsson, O., Dyer, P.S., and Miao, V. 2013. Lichen genomics: prospects and progress. In Ecological genomics of fungi. Edited by Francis Martin. Wiley-Blackwell, Oxford, UK. pp. 191-212.
23. Gueidan, C., Savic, S., Thüs, H., Roux, C., Keller, C., Tibell, L., et al. 2009.Generic classification of the Verrucariaceae (Ascomycota) based on molecular and morphological evidence: recent progress and remaining challenges. Taxon, 58(1): 184-208.
24. Haas, J.R., and Purvis, W.O. 2006. Lichen biogeochemistry. In Fungi in biogeochemical cycles. Edited by G.M. Gadd. Cambridge University, Cambridge, UK. pp. 344-376.
25. Henckel, P.A., and Plotnikova, T.T. 1973. Nitrogen-fixing bacteria in lichens. Izv. Akad. Nauk SSSR Ser. Biol. 1973: 807-813. PMID:4779562. In Russian.
26. Henckel, P.A., and Yuzhakova, L.A. 1936. On the role of Azotobacter in the lichen symbiosis. Izv. Biol. Inst. Permsk. Gos. Univ. 10: 9-10.
27. Hirsch, P., Ludwig, W., Hethke, C., Sittig, M., Hoffmann, B., and Gallikowski, C.A. 1998. Hymenobacter roseosalivarius gen. nov., sp. nov. from continental Antarctic soils and sandstone: bacteria of the Cytophaga/Flavobacterium/Bacteroides line of phylogenetic descent. Syst. Appl. Microbiol. 21: 374-383. doi:10.1016/ S0723-2020(98)80047-7. PMID:9841127.
28. Hodkinson, B.P., and Lutzoni, F. 2009. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis, 49(3): 163-180. doi:10.1007/s13199-009-0049-3.
29. Hodkinson, B.P., Gottel, N.R., Schadt, C.W., and Lutzoni, F. 2012. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ. Microbiol. 14(1): 147-161. doi:10.1111/j.1462-2920.2011.02560.x. PMID:21906220.
30. Johnson, K.S., and Petty, R.L. 1983. Determination of nitrate and nitrite in seawater by flow injection analysis. Limnol. Oceanol. 28: 1260-1266. doi:10.4319/ lo.1983.28.6.1260.
31. Kersters, K., de Vos, P., Gillis, M., Swings, J., Vandamme, P., and Stackebrandt, E. 2006. Introduction to the Proteobacteria. Prokaryotes, 5: 3-37. doi:10.1007/0-387-30745-1-1.
32. Khan, S.T., Fukunaga, Y., Nakagawa, Y., and Harayama, S. 2007. Emended descriptions of the genus Lewinella and of Lewinella cohaerens, Lewinella nigricans and Lewinella persica, and description of Lewinella lutea sp. nov. and Lewinella marina sp. nov. Int. J. Syst. Evol. Microbiol. 57: 2946-2951. doi:10.1099/ijs.0. 65308-0. PMID:18048755.
33. Kim, B.-S., Lim, Y.W., and Chun, J. 2008a. Sphingopyxis marina sp. nov. and Sphingopyxis litioris sp. nov., isolated from seawater. Int. J. Syst. Evol. Microbiol. 58(10): 2415-2419. doi:10.1099/ijs.0.65614-0. PMID:18842866.
34. Kim, B.-Y., Yoo, S.-H., Weon, H.-Y., Jeon, Y.-A., Hong, S.-B., Go, S.-J., et al. 2008b. Jannaschia pohangensis sp. nov., isolated from seashore sand in Korea. Int. J. Syst. Evol. Microbiol. 58: 496-499. doi:10.1099/ijs.0.65167-0. PMID:18218956.
35. Kirchman, D.L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39: 91-100. doi:10.1111/j.1574-6941.2002. tb00910.x. PMID:19709188.
36. Kwon, K., Woo, J., Yang, S., Kang, J., Kang, S.G., Kim, S., et al. 2007. Altererythro-bacterepoxidivoransgen. nov., sp. nov., an epoxide hydrolase-active, mesophilic marine bacterium isolated from cold-seep sediment, and reclassification of Erythrobacter luteolus Yoon et al. 2005 as Altererythrobacter luteolus comb. nov. Int. J. Syst. Evol. Microbiol. 57: 2207-2211. doi:10.1099/ijs.0.64863-0. PMID: 17911284.
37. Liba, C.M., Ferrara, F.I.S., Manfio, G.P., Fantinatti-Garboggini, F., Albuquerque, R.C., Pavan, C., et al. 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. doi:10.1111/j.1365-2672.2006.03010.x. PMID:17040231.
38. Macián, M.C., Arahal, D.R., Garay, E., Ludwig, W., Schleifer, K.H., and Pujalte, M.J. 2005. Jannaschia rubra sp. nov., a red-pigmented bacterium isolated from sea water. Int. J. Syst. Evol. Microbiol. 55: 649-653. doi:10.1099/ijs. 0.63412-0. PMID:15774638.
39. McIntosh, D., Ji, B., Forward, B.S., Puvanendran, V., Boyce, D., and Ritchie, R. 2008. Culture-independent characterization of the bacterial populations associated with cod (Gadus morhua L.) and live feed at an experimental hatchery facility using denaturing gradient gel electrophoresis. Aquaculture, 275: 42-50. doi:10.1016/j.aquaculture.2007.12.021.
40. Muyzer, G., de Waal, E.C., and Uitterlinden, A.G. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695-700. PMID:7683183.
41. Nautiyal, C.S. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170: 265-270. doi:10.1111/j.1574-6968.1999.tb13383.x. PMID:9919677.
42. Nedashkovskaya, O.I., Kim, S.B., Lysenko, A.M., Frolova, G.M., Mikhailov, V.V., Lee, K.H., and Bae, K.S. 2005. Description of Aquimarina muelleri gen. nov., sp. nov., and proposal of the reclassification of [Cytophaga] latercula Lewin 1969 as Stanierella latercula gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 55: 225-229. doi:10.1099/ijs.0.63349-0. PMID:15653878.
43. Nedashkovskaya, O.I., Vancanneyt, M., Christiaens, L., Kalinovskaya, N.I., Mikhailov, V.V., and Swings, J. 2006. Aquimarina intermedia sp. nov., reclassification of Stanierella latercula (Lewin 1969) as Aquimarina latercula comb. nov. and Gaetbulimicrobium brevivitae Yoon et al. 2006 as Aquimarina brevivitae comb. nov. and emended description of the genus Aquimarina. Int. J. Syst. Evol. Microbiol. 56: 2037-2041. doi:10.1099/ijs.0.64155-0. PMID:16957096.
44. Notomista, E., Pennacchio, F., Cafaro, V., Smaldone, G., Izzo, V., Troncone, L., et al. 2011. The marine isolate Novosphingobium sp. PP1Y shows specific adaptation to use the aromatic fraction of fuels as the sole carbon and energy source. Microb. Ecol. 61(3): 582-594. doi:10.1007/s00248-010-9786-3. PMID: 21258788.
45. Oren, A. 2006. The genera Rhodothermus, Thermonema, Hymenobacter and Salinibacter. Prokaryotes 7: 712-738. doi:10.1007/0-387-30747-8-29.
46. Pangallo, D., Šimonovičová, A., Chovanocá, K., and Ferianc, P. 2007. Wooden art objects and the museum environment: identification and biodegradative characteristics of isolated microflora. Lett. Appl. Microbiol. 45(1): 87-94. doi: 10.1111/j.1472-765X.2007.02138.x. PMID:17594466.
47. Ravenschlag, K., Sahm, K., and Amann, R. 2001. Quantitative molecular analysis of the microbial community in marine Arctic sediments (Svalbard). Appl. Environ. Microbiol. 67: 387-395. doi:10.1128/AEM.67.1.387-395.2001. PMID: 11133470.
48. Reichenbach, H. 2006. The order Cytophagales. Prokaryotes, 7: 549-590. doi:10. 1007/0-387-30747-8-20.
49. Rodríguez, H., and Fraga, R. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319-339. doi:10.1016/S0734-9750(99)00014-2. PMID:14538133.
50. Scott, G.D. 1956. Further investigation of some lichens for fixation of nitrogen. New Phytol. 55(1): 111-116. doi:10.1111/j.1469-8137.1956.tb05269.x.
51. Selbmann, L., Zucconi, L., Ruisi, S., Grube, M., Cardinale, M., and Onofri, S. 2010. Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance. Polar Biol. 33: 71-83. doi:10.1007/s00300-009-0686-2.
52. Shade, A., Hogan, C.S., Klimowicz, A.K., Linske, M., McManus, P.S., and Handelsman, J. 2012. Culturing captures members of the soil rare biosphere. Environ. Mircobiol. 14(9): 2247-2252. doi:10.1111/j.1462-2920.2012.02817.x. PMID:22788977.
53. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739. doi:10.1093/molbev/msr121. PMID:21546353.
54. Tehler, A., and Wedin, M. 2008. Systematics and lichenized fungi. In Lichen biology. Edited by T.H. Nash III. 2nd ed. Cambridge University Press, Cambridge, UK. pp. 336-352.
55. Tindall, B.J., Sikorski, J., Smibert, R.A., and Krieg, N.R. 2007. Phenotypic characterization and the principles of comparative systematics. In Methods for general and molecular microbiology. Edited by C.A. Reddy. ASM Press, Washington D.C., USA. pp. 330-393.
56. Ting, L., Williams, T.J., Cowley, M.J., Lauro, F.M., Guilhaus, M., Raftery, M.J., and Cavicchioli, R. 2010. Cold adaptation in the marine bacterium Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ. Microbiol. 12: 2658-2676. doi:10.1111/j.1462-2920.2010.02235.x. PMID:20482592.
57. Trappen, S.V., Mergaert, J., and Swings, J. 2004. Loktanella salsiacus gen. nov., sp. nov., Loktanella fryxellensis sp. nov. and Loktanella vestfoldensis sp. nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. Int. J. Syst. Evol. Microbiol. 54: 1263-1269. PMID:15280301.
58. Wagner-Döbler, I., Rheims, H., Felske, A., Pukall, R., and Tindall, B.J. 2003. Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea. Int. J. Syst. Evol. Microbiol. 53: 731-738. doi:10.1099/ijs.0.02377-0. PMID:12807194.
59. Yoon, J., Kang, K.H., Yeo, S., and Oh, T. 2005. Erythrobacter luteolus sp. nov., isolated from a tidal flat of the Yellow Sea in Korea. Int. J. Syst. Evol. Microbiol. 55: 1167-1170. doi:10.1099/ijs.0.63522-0. PMID:15879250.