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Phylogeographic analysis of filterable bacteria with special reference to Rhizobiales strains that occur in cryospheric habitats

Published online by Cambridge University Press:  20 March 2013

Ryosuke Nakai
Affiliation:
Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-hiroshima, Hiroshima 739-8528, Japan Research Fellow of the Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo 102-8471, Japan
Eri Shibuya
Affiliation:
Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-hiroshima, Hiroshima 739-8528, Japan
Ana Justel
Affiliation:
Departamento de Matemáticas, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Eugenio Rico
Affiliation:
Departamento de Ecología, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Antonio Quesada
Affiliation:
Departamento de Biología, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Fumihisa Kobayashi
Affiliation:
Institute of Nature and Environmental Technology, Kanazawa University, Kakuma-machi, Kanazawa 920-1192, Japan
Yasunobu Iwasaka
Affiliation:
Institute of Nature and Environmental Technology, Kanazawa University, Kakuma-machi, Kanazawa 920-1192, Japan
Guang-Yu Shi
Affiliation:
Institute of Atmospheric Physics, Chinese Academy of Science, Beijing 100029, China
Yuki Amano
Affiliation:
Japan Atomic Energy Agency, Mizunami Underground Research Laboratory, 1-64 Yamanouchi, Akeyo-cho, Mizunami-shi, Gifu 509-6132, Japan Japan Atomic Energy Agency, Horonobe Underground Research Center, Hokushin 432-2, Horonobe-cho, Teshio-Gun, Hokkaido 098-3224, Japan
Teruki Iwatsuki
Affiliation:
Japan Atomic Energy Agency, Mizunami Underground Research Laboratory, 1-64 Yamanouchi, Akeyo-cho, Mizunami-shi, Gifu 509-6132, Japan Japan Atomic Energy Agency, Horonobe Underground Research Center, Hokushin 432-2, Horonobe-cho, Teshio-Gun, Hokkaido 098-3224, Japan
Takeshi Naganuma*
Affiliation:
Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-hiroshima, Hiroshima 739-8528, Japan
*
*corresponding author: takn@hiroshima-u.ac.jp

Abstract

Although the lower size limit of microorganisms was previously believed to be c. 0.2 μm, there is evidence for the existence of microorganisms that can pass through 0.2 μm-pore-size filters called ultramicrobacteria or nanobacteria. However, information on the phylogeny and biogeography of these bacteria is limited. We obtained 53 isolates of 0.2 μm-passable bacteria from 31 samples collected at 26 locations worldwide, including the Arctic Svalbard Islands, deserts, and Maritime Antarctica. Phylogenetic analysis of near full-length 16S rRNA gene sequences revealed that 18 of the 53 isolates were < 97% homologous with previously cultured isolates, representing potentially novel species. Two isolates (order Rhizobiales) (100% identical) collected from Byers Peninsula, Livingston Island in Maritime Antarctica, were closely related (99.8% similarity) to an isolate collected from intertidal sediments in East Antarctica. In addition, the sequence of this Antarctic isolate showed ≥ 97% similarity to 901 sequences derived from known isolates and samples collected at geographically disparate locations under various environmental conditions. Interestingly, among 13 sequences showing ≥ 99% similarity, ten were isolated from cryospheric habitats such as Arctic, Antarctic, and alpine environments. This implies that such Rhizobiales strains occur in the cryospheric regions, however, their abundance and biomass may be scarce depending on the geographic location.

Type
Research Articles
Copyright
Copyright © Antarctic Science Ltd 2013

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References

Aljanabi, S.M.Martinez, I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 46924693.CrossRefGoogle ScholarPubMed
Baas-Becking, L.G.M. 1934. Geobiologie of inleiding tot de milieukunde. The Hague: Van Stockum and Zoon, 263 pp.Google Scholar
Chen, B., Kobayashi, F., Yamada, M., Kim, Y., Iwasaka, Y.Shi, G. 2011. Identification of culturable bioaerosols collected over dryland in northwest China: observation using a tethered balloon. Asian Journal of Atmospheric Environment, 5, 172180.CrossRefGoogle Scholar
DeLong, E.F. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Science of the United States of America, 89, 56855869.CrossRefGoogle ScholarPubMed
DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P.Andersen, G.L. 2006. Greengenes: chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72, 50695072.CrossRefGoogle ScholarPubMed
Dmitriev, V.V., Duda, V.I., Suzina, N.E., Akimov, V.N., Vainshtein, M.B., Barinova, E.S., Abashina, T.N., Oleynikov, R.R., Esikova, T.Z.Boronin, A.M. 2007. Ultrastructural organization and development cycle of soil ultramicrobacteria belonging to the class Alphaproteobacteria. Microbiology, 76, 575584.Google Scholar
Elsaied, H.E., Sato, M.Naganuma, T. 2001. Viable Cytophaga-like bacterium in the 0.2 μm-filtrate seawater. Systematic and Applied Microbiology, 24, 618622.CrossRefGoogle Scholar
Fukuba, T., Elsaied, H.E.Naganuma, T. 2002. Overlooked microbial agents in aquaculture: nanobacteria. In Lee, C.S. & O'Bryen, P., eds. Microbial approaches to aquatic nutrition within environmentally sound aquaculture production systems. Baton Rouge, LA: World Aquaculture Society, 99107.Google Scholar
Geissinger, O., Herlemann, D.P., Morschel, E., Maier, U.G.Brune, A. 2009. The ultramicrobacterium “Elusimicrobium minutum” gen. nov., sp. nov., the first cultivated representative of the termite group 1 phylum. Applied Environmental Microbiology, 75, 28312840.CrossRefGoogle ScholarPubMed
Green, J.Bohannan, B.J. 2006. Spatial scaling of microbial biodiversity. Trends in Ecology & Evolution, 21, 501507.CrossRefGoogle ScholarPubMed
Hahn, M.W. 2003. Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Applied Environmental Microbiology, 69, 52485254.CrossRefGoogle Scholar
Hahn, M.W. 2004. Broad diversity of viable bacteria in ‘sterile’ (0.2 μm) filtered water. Research in Microbiology, 155, 688691.CrossRefGoogle Scholar
Hahn, M.W., Stadler, P., Wu, Q.L.Pockl, M. 2004. The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. Journal of Microbiological Methods, 57, 379390.CrossRefGoogle Scholar
Hahn, M.W., Lang, E., Brandt, U., Wu, Q.L.Scheuerl, T. 2009. Emended description of the genus Polynucleobacter and the species Polynucleobacter necessarius and proposal of two subspecies, P. necessarius subsp. necessarius subsp. Nov. and P. necessarius subsp. asymbioticus subsp. nov. International Journal of Systematic and Evolutionary Microbiology, 59, 20022009.CrossRefGoogle ScholarPubMed
Hahn, M.W., Lunsdorf, H., Wu, Q.L., Schauer, M., Hofle, M.G., Boenigk, J.Stadler, P. 2003. Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Applied Environmental Microbiology, 69, 14421451.CrossRefGoogle ScholarPubMed
Haller, C.M., Rolleke, S., Vybiral, D., Witte, A.Velimirov, B. 2000. Investigation of 0.2 μm filterable bacteria from the western Mediterranean Sea using a molecular approach: dominance of potential starvation forms. FEMS Microbiology Ecology, 31, 153161.Google Scholar
Hobbie, J.E., Daley, R.J.Jasper, S. 1977. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology, 33, 12251228.CrossRefGoogle Scholar
Hood, M.A.MacDonell, M.T. 1987. Distribution of ultramicrobacteria in a gulf-coast estuary and induction of ultramicrobacteria. Microbial Ecology, 14, 113127.CrossRefGoogle Scholar
Jamtveit, B., Hammer, O., Andersson, C., Dysthe, D.K., Heldmann, J.Vogel, M.L. 2006. Travertines from the Troll thermal springs, Svalbard. Norwegian Journal of Geology, 86, 387395.Google Scholar
Kumar, S., Tamura, K., Dudley, J.Nei, M. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 15961599.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J.Higgins, D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23, 29472948.CrossRefGoogle ScholarPubMed
MacDonell, M.T.Hood, M.A. 1982. Isolation and characterization of ultramicrobacteria from a gulf coast estuary. Applied and Environmental Microbiology, 43, 566571.CrossRefGoogle ScholarPubMed
Maniloff, J. 1997. Nanobacteria: size limits and evidence. Science, 276, 1776.CrossRefGoogle Scholar
Martiny, J.B.H., Bohannan, B.J.M., Brown, J.H., Colwell, R.K., Fuhrman, J.A., Green, J.L., Horner-Devine, M.C., Kane, M., Krumins, J.A., Kuske, C.R., Morin, P.J., Naeem, S., Øvreås, L., Reysenbach, A-L., Smith, V.H.Staley, J.T. 2006. Microbial biogeography: putting microorganisms on the map. Nature Reviews Microbiology, 4, 102112.CrossRefGoogle ScholarPubMed
Massa, S., Caruso, M., Trovatelli, F.Tosques, M. 1998. Comparison of plate count agar and R2A medium for enumeration of heterotrophic bacteria in natural mineral water. World Journal of Microbiology & Biotechnology, 14, 727730.CrossRefGoogle Scholar
Miteva, V.I.Brenchley, J.E. 2005. Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Applied and Environmental Microbiology, 71, 78067818.CrossRefGoogle ScholarPubMed
Miyoshi, T., Iwatsuki, T.Naganuma, T. 2005. Phylogenetic characterization of 16S rRNA gene clones from deep-groundwater microorganisms that pass through 0.2 micrometer-pore-size filters. Applied and Environmental Microbiology, 71, 10841088.CrossRefGoogle ScholarPubMed
Mushegian, A.R.Koonin, E.V. 1996. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proceedings of the National Academy of Science of the United States of America, 93, 10 26810 273.CrossRefGoogle ScholarPubMed
Naganuma, T., Miyoshi, T.Kimura, H. 2007. Phylotype diversity of deep-sea hydrothermal vent prokaryotes trapped by 0.2 and 0.1-μm-pore-size filters. Extremophiles, 11, 637646.CrossRefGoogle ScholarPubMed
Nakai, R., Abe, T., Takeyama, H.Naganuma, T. 2011. Metagenomic analysis of 0.2 μm-passable microorganisms in deep-sea hydrothermal fluid. Marine Biotechnology, 13, 900908.CrossRefGoogle ScholarPubMed
Pearce, D.A., Cockell, C.S., Lindstrom, E.S.Tranvik, L.J. 2007. First evidence for a bipolar distribution of dominant freshwater lake bacterioplankton. Antarctic Science, 19, 245252.CrossRefGoogle Scholar
Pedrós-Alió, C. 2006. Marine microbial diversity: can it be determined? Trends in Microbiology, 14, 257263.CrossRefGoogle ScholarPubMed
Postma, J., Vanelsas, J.D., Govaert, J.M.Vanveen, J.A. 1988. The dynamics of Rhizobium leguminosarum biovar. trifolii introduced into soil as determined by immunofluorescence and selective plating techniques. FEMS Microbiology Ecology, 53, 251259.Google Scholar
Quesada, A., Camacho, A., Rochera, C.Velázquez, D. 2009. Byers Peninsula: a reference site for coastal, terrestrial and limnetic ecosystem studies in Maritime Antarctica. Polar Science, 3, 181187.CrossRefGoogle Scholar
Torrella, F.Morita, R.Y. 1981. Microcultural study of bacterial size changes and microcolony and ultramicrocolony formation by heterotrophic bacteria in seawater. Applied and Environmental Microbiology, 41, 518527.CrossRefGoogle ScholarPubMed
Wang, Y., Hammes, F., Boon, N.Egli, T. 2007. Quantification of the filterability of freshwater bacteria through 0.45, 0.22, and 0.1 μm pore size filters and shape-dependent enrichment of filterable bacterial communities. Environmental Science & Technology, 41, 70807086.CrossRefGoogle Scholar
Watson, S.W., Novitsky, T.J., Quinby, H.L.Valois, F.W. 1977. Determination of bacterial number and biomass in the marine environment. Applied and Environmental Microbiology, 33, 940946.CrossRefGoogle ScholarPubMed
Yu, Y., Li, H.R., Zeng, Y.X.Chen, B. 2010. Phylogenetic diversity of culturable bacteria from Antarctic sandy intertidal sediments. Polar Biology, 33, 869875.CrossRefGoogle Scholar
Zimmermann, R. 1977. Estimation of bacterial number and biomass by epifluorescence microscopy and scanning electron microscopy. In Rheinheimer, G., ed. Microbial ecology of a brackish water environment. Berlin: Springer, 103120.CrossRefGoogle Scholar