The Variation of Microbial Communities in a Depth Profile of an Acidic, Nutrient-Poor Boreal Bog in Southwestern Finland

Abstract

Natural bacterial communities impact the motility of isotopes, such as radionuclides, in the environment. As a result of post glacial crustal rebound radionuclides may escape the deep geological repository for spent nuclear fuel on Olkiluoto Island, Finland, and reach surface environments. Lastensuo Bog, a 5300-year-old raised bog in southwestern Finland, functions as analogue ecotope for bogs formed in Olkiluoto due to the crustal rebound. A core comprising the depth profile (0 - 7 m depth) of the bog including surface Sphagnum moss, peat and bottom clay was obtained using a stainless steel corer. High throughput sequencing was used to characterize the bacterial communities throughout the bog’s depth profile. A total of 12,680 bacterial Operational Taxonomic Units (OTUs) (97% sequence similarity) were detected comprising altogether 40 different bacterial phyla. Of these, 13 phyla were present at all depths, accounting for 97% - 99% of the whole bacterial community. The bacterial communities differed notably through the bog’s depth profile, dividing it into five distinct strata: 1) the Sphagnum moss layer; 2) 0.5 - 3.7 m; 3) 3.7 - 4.0 m; 4) 5.5 - 6.0 m deep peat; 5) the former seabed clay at 6.5 - 7.0 m depth. Acidobacteria, α- and γ-Proteobacteria dominated the surface community, but in the peat Acidobacteria contributed with up to 85% of the bacterial community. The estimated bacterial population density ranged between 2 × 109 and 5 × 1010 16S rRNA gene copies g-1 dry-weight peat. This study revealed that Lastensuo Bog had a highly diverse bacterial community. Most of the taxonomic groups belonged to thus far poorly characterized and uncultured bacteria with unknown physiological role. However, new insights into the distribution of bacterial taxa and their putative roles in organic carbon break down within the bog ecosystem have been obtained and an important baseline for further studies has been established.

Share and Cite:

Tsitko, I. , Lusa, M. , Lehto, J. , Parviainen, L. , Ikonen, A. , Lahdenperä, A. and Bomberg, M. (2014) The Variation of Microbial Communities in a Depth Profile of an Acidic, Nutrient-Poor Boreal Bog in Southwestern Finland. Open Journal of Ecology, 4, 832-859. doi: 10.4236/oje.2014.413071.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Bridgham, S.D., Megonigal, J.P., Keller, J.K., Bliss, N.B. and Trettin, C. (2006) The Carbon Balance of North American Wetlands. Wetlands, 26, 889-916.
http://dx.doi.org/10.1672/0277-5212(2006)26[889:TCBONA]2.0.CO;2
[2] Smith, L.C., Macdonald, G.M., Velichko, A.A., Beilman, D.W., Borisova, O.K., Frey, K.E., Kremenetski, K.V. and Sheng, Y. (2004) Siberian Peatlands a Net Carbon Sink and Global Methane Source Since the Early Holocene. Science, 303, 353-356. http://dx.doi.org/10.1126/science.1090553
[3] Dean, W.E. and Gorham, E. (1998) Magnitude and Significance of Carbon Burial in Lakes, Reservoirs, and Peatlands. Geology, 26, 535-538.
http://dx.doi.org/10.1130/0091-7613(1998)026<0535:MASOCB>2.3.CO;2
[4] Turunen, J., Tomppo, E., Tolonen, K. and Reinikainen, A. (2002) Estimating Carbon Accumulation Rate of Undrained Mires in Finland—Application to Boreal and Subarctic Regions. The Holocene, 12, 69-80.
http://dx.doi.org/10.1191/0959683602hl522rp
[5] Conrad, R. (2009) The Global Methane Cycle: Recent Advances in Understanding the Microbial Processes Involved. Environmental Microbiology Reports, 1, 285-292.
http://dx.doi.org/10.1111/j.1758-2229.2009.00038.x
[6] Virtanen, K. and Valpola, S. (2011) Energy Potential of Finnish Peatlands. In: Nenonen, K. and Nurmi, P.A., Eds., Geoscience for Society, Vol. 125, Geological Survey of Finland, Special Paper 49, Espoo, 153-161.
[7] Coulson, J.C. and Butterfield, J. (1978) An Investigation of the Biotic Factors Determining the Rates of Plant Decomposition on Blanket Bog. Journal of Ecology, 66, 631-650.
http://dx.doi.org/10.2307/2259155
[8] Scheffer, R.A., Van Logtestijn, R.S. and Verhoeven, J.T.A. (2001) Decomposition of Carex and Sphagnum Litter in Two Mesotrophic Fens Differing in Dominant Plant Species. Oikos, 92, 44-54.
http://dx.doi.org/10.1034/j.1600-0706.2001.920106.x
[9] Posiva (2012) Safety Case for the Disposal of Spent Nuclear Fuel at Olkiluoto—Description of the Disposal System 2012. Report POSIVA 2012-05, Posiva Oy, Eurajoki, 166 p. http://www.posiva.fi/
[10] Makiaho, J.P. (2005) Development of Shoreline and Topography in the Olkiluoto Area, Western Finland, 2000 BP8000 AP. Working Report 2005-70, Posiva Oy, Eurajoki, 47 p. http://www.posiva.fi
[11] Haapanen, R., Aro, L., Helin, J., Ikonen, A.T.K. and Lahdenpera, A.M. (2013) Studies on Reference Mires: 1. Lastensuo and Pesansuo in 2010-2011. Working Report 2012-102, Posiva Oy, Eurajoki.
[12] Posiva (2013) Safety Case for the Disposal of Spent Nuclear Fuel at Olkiluoto—Biosphere Assessment 2012. Report POSIVA 2012-10, Posiva Oy, Eurajoki, 251 p. http://www.posiva.fi/
[13] Haapanen, R., Aro, L., Koivunen, S., Lahdenpera, A.M., Kirkkala, T., Hakala, A., Helin, J. and Ikonen, A.T.K. (2011) Selection of Real-Life Analogues for Future Lakes and Mires at a Repository Site. Radioprotection, 46, S647-S651.
http://dx.doi.org/10.1051/radiopro/20116660s
[14] Andersen, R., Chapman, S.J. and Artz, R.R.E. (2013) Microbial Communities in Natural and Disturbed Peatlands: A Review. Soil Biology and Biochemistry, 57, 979-994.
http://dx.doi.org/10.1016/j.soilbio.2012.10.003
[15] Dedysh, S.N. (2011) Cultivating Uncultured Bacteria from Northern Wetlands: Knowledge Gained and Remaining Gaps. Frontiers in Microbiology, 2, 184. http://dx.doi.org/10.3389/fmicb.2011.00184
[16] Sharp, C.E., Smirnova, A.V., Graham, J.M., Stott, M.B., Khadka, R., Moore, T.R., Grasby, S.E., Strack, M. and Dunfield, P.F. (2014) Distribution and Diversity of Verrucomicrobia Methanotrophs in Geothermal and Acidic Environments. Environmental Microbiology, 16, 1867-1878. http://dx.doi.org/10.1111/1462-2920.12454
[17] Kip, N., Van Winden, J., Pan, Y., Bodrossy, L., Reichart, G.J., Smolders, A.J.P., Jetten, M.S.M., Sinninghe Damsté, J.S. and Op den Camp, H.J.M. (2010) Global Prevalence of Methane Oxidation by Symbiotic Bacteria in Peat-Moss Ecosystems. Nature Geoscience, 3, 617-621. http://dx.doi.org/10.1038/ngeo939
[18] Juottonen, H., Galand, P.E., Tuittila, E.S., Laine, J., Fritze, H. and Yrjala, K. (2005) Methanogen Communities and Bacteria along an Ecohydrological Gradient in a Northern Raised Bog Complex. Environmental Microbiology, 7, 1547-1557. http://dx.doi.org/10.1111/j.1462-2920.2005.00838.x
[19] Sun, H., Terhonen, E., Koskinen, K., Paulin, L., Kasanen, R. and Asiegbu, F.O. (2014) Bacterial Diversity and Community Structure along Different Peat Soils in Boreal Forest. Applied Soil Ecology, 74, 37-45.
http://dx.doi.org/10.1016/j.apsoil.2013.09.010
[20] Morales, S.E., Mouser, P.J., Ward, N., Hudman, S.P., Gotelli, N.J., Ross, D.S. and Lewis, T.A. (2006) Comparison of Bacterial Communities in New England Sphagnum Bogs Using Terminal Restriction Fragment Length Polymorphism (T-RFLP). Microbial Ecology, 52, 34-44. http://dx.doi.org/10.1007/s00248-005-0264-2
[21] Palmer, K., Biasi, C. and Horn, M.A. (2011) Contrasting Denitrifier Communities Relate to Contrasting N2O Emission Patterns from Acidic Peat Soils in Arctic Tundra. The ISME Journal, 6, 1058-1077.
http://dx.doi.org/10.1038/ismej.2011.172
[22] Lin, X., Green, S., Tfaily, M.M., Prakash, O., Konstantinidis, K.T., Corbett, J.E., Chanton, J.P., Cooper, W.T. and Kostka, J.E. (2012) Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland. Applied and Environmental Microbiology, 78, 7023-7031. http://dx.doi.org/10.1128/AEM.01750-12
[23] Lin, X., Tfaily, M.M., Steinweg, J.M., Chanton, P., Esson, K., Yang, Z.K., Chanton, J.P., Cooper, W., Schadt, C.W. and Kostka, J.E. (2014) Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA. Applied and Environmental Microbiology, 80, 3518-3530. http://dx.doi.org/10.1128/AEM.00205-14
[24] Serkebaeva, Y.M., Kim, Y., Liesack, W. and Dedysh, S.N. (2013) Pyrosequencing-Based Assessment of the Bacteria Diversity in Surface and Subsurface Peat Layers of a Northern Wetland, with Focus on Poorly Studied Phyla and Candidate Divisions. PLoS ONE, 8, e63994.
[25] Makila, M. and Grundstrom, A. (2008) Turpeenika Ja Kerrostumisnopeuslounais-Suomensoilla. Working Report 2008-12, Posiva Oy, Eurajoki.
[26] Lusa, M., Ammala, K., Hakanen, M., Lehto, J. and Lahdenpera, A.M. (2009) Chemical and Geotechnical Analyses of Soil Samples from Olkiluoto for Studies on Sorption in Soils. Working Report 2009-33, Posiva Oy, Eurajoki.
[27] Carter, M.R. and Gregorich, E.G. (2008) Soil Sampling and Methods of Analysis. 2nd Edition, Canadian Society of Soil Science, Taylor & Francis Group, LLC, Boca Raton.
[28] Edwards, U., Rogall, T., Blocker, H., Emde, M. and Bottger, E.C. (1998) Isolation and Direct Complete Nucleotide Determination of Entire Genes. Characterization of a Gene Coding for 16S Ribosomal RNA. Nucleic Acids Research, 17, 7843-7853. http://dx.doi.org/10.1093/nar/17.19.7843
[29] 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. Applied and Environmental Microbiology, 59, 695-700.
[30] Bomberg, M. and Itavaara, M. (2012) The Diversity of Microbial Communities in Olkiluoto Groundwater Fracture Zones Characterized by DNA and RNA Based 16S rRNA-Targeted 454 Pyro Sequencing and qPCR. Posiva Working Report 2012-27, Posiva Oy, Eurajoki.
[31] Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Knight, R., et al. (2010) QIIME Allows Analysis of High-Throughput Community Sequencing Data. Nature Methods, 7, 335-336.
http://dx.doi.org/10.1038/nmeth.f.303
[32] Desantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G.L. (2006) Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Applied and Environmental Microbiology, 72, 5069-5072. http://dx.doi.org/10.1128/AEM.03006-05
[33] Langille, M.G.I., Zaneveld, J., Caporaso, J.G., Mcdonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Vega Thurber, R.L., Knight, R., Beiko, R.G. and Huttenhower, C. (2013) Predictive Functional Profiling of Microbial Communities Using 16S rRNA Marker Gene Sequences. Nature Biotechnology, 31, 814-821.
[34] Goecks, J., Nekrutenko, A. and Taylor, J., the Galaxy Team (2010) Galaxy: A Comprehensive Approach for Supporting Accessible, Reproducible, and Transparent Computational Research in the Life Sciences. Genome Biology, 11, R86. http://dx.doi.org/10.1186/gb-2010-11-8-r86
[35] Blankenberg, D., Von Kuster, G., Coraor, N., Ananda, G., Lazarus, R., Mangan, M., Nekrutenko, A. and Taylor, J. (2010) Galaxy: A Web-Based Genome Analysis Tool for Experimentalists. Current Protocols in Molecular Biology, Chapter 19: Unit 19.10.1-21.
[36] Giardine, B., Riemer, C., Hardison, R.C., Burhans, R., Elnitski, L., Shah, P., Zhang, Y., Blankenberg, D., Albert, I., Taylor, J., Miller, W., Kent, W.J. and Nekrutenko, A. (2005) Galaxy: A Platform for Interactive Large-Scale Genome Analysis. Genome Research, 15, 1451-1455.
http://dx.doi.org/10.1101/gr.4086505
[37] Barns, S.M., Cain, E.C., Sommerville, L. and Kuske, C.R. (2007) Acidobacteria Phylum Sequences in Uranium-Contaminated Subsurface Sediments Greatly Expand the Known Diversity within the Phylum. Applied and Environmental Microbiology, 73, 3113-3116. http://dx.doi.org/10.1128/AEM.02012-06
[38] Dedysh, S.N., Pankratov, T.A., Belova, S.E., Kulichevskaya, I.S. and Liesack, W. (2006) Phylogenetic Analysis and in Situ Identification of Bacteria Community Composition in an Acidic Sphagnum Peat Bog. Applied and Environmental Microbiology, 72, 2110-2117. http://dx.doi.org/10.1128/AEM.72.3.2110-2117.2006
[39] Mannisto, M.K., Rawat, S., Starovoytov, V. and Haggblom, M.M. (2012) Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov. and granulicella sapmiensis sp. nov., Novel Acidobacteria from Tundra Soil. International Journal of Systematic and Evolutionary Microbiology, 62, 2097-2106.
http://dx.doi.org/10.1099/ijs.0.031864-0
[40] Pankratov, T.A. and Dedysh, S.N. (2010) Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and granulicella rosea sp. nov., Acidophilic, Polymer-Degrading Acidobacteria from Sphagnum Peat Bogs. International Journal of Systematic and Evolutionary Microbiology, 60, 2951-2959.
http://dx.doi.org/10.1099/ijs.0.021824-0
[41] Pankratov, T.A., Ivanova, A.O., Dedysh, S.N. and Liesack, W. (2011) Bacterial Populations and Environmental Factors Controlling Cellulose Degradation in an Acidic Sphagnum Peat. Environmental Microbiology, 13, 1800-1814.
http://dx.doi.org/10.1111/j.1462-2920.2011.02491.x
[42] Ward, N.L., Challacombe, J.F., Janssen, P.H., Henrissat, B., Coutinho, P.M., Wu, M., Kuske, C.R., et al. (2009) Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils. Applied and Environmental Microbiology, 75, 2046-2056.
http://dx.doi.org/10.1128/AEM.02294-08
[43] Pankratov, T.A., Kirsanova, L.A., Kaparullina, E.N., Kevbrin, V.V. and Dedysh, S.N. (2012) Telmatobacter bradus gen. nov., sp. nov., a Cellulolytic Facultative Anaerobe from Subdivision 1 of the Acidobacteria, and Emended Description of Acidobacterium capsulatum kishimoto et al. 1991. International Journal of Systematic and Evolutionary Microbiology, 62, 430-437. http://dx.doi.org/10.1099/ijs.0.029629-0
[44] Rheims, H., Rainey, F.A. and Stackebrandt, E. (1996) A Molecular Approach to Search for Diversity among Bacteria in the Environment. Journal of Industrial Microbiology, 17, 159-169.
http://dx.doi.org/10.1007/BF01574689
[45] García-Moyano, A., Gonzáles-Toril, E., Aguilera, A. and Amils, R. (2007) Prokaryotic Community Composition and Ecology of Floating Macroscopic Filaments from an Extreme Acidic Environment, RíO Tinto (SW, Spain). Systematic and Applied Microbiology, 30, 601-614.
http://dx.doi.org/10.1016/j.syapm.2007.08.002
[46] Kimoto, K.I., Aizawa, T., Urai, M., Ve, N.B., Suzuki, K.I., Nakajima, M. and Sunairi, M. (2010) Acidocella aluminiidurans sp. nov., an Aluminium-Tolerant Bacterium Isolated from Panicum repens Grown in a Highly Acidic Swamp in Actual Acid Sulfate Soil Area of Vietnam. International Journal of Systematic and Evolutionary Microbiology, 60, 764-768. http://dx.doi.org/10.1099/ijs.0.011569-0
[47] Wichlacz, P.L., Unz, R.F. and Langworthy, T.A. (1986) Acidiphilium angustum sp. nov., Acidiphilium facilis sp. nov., and Acidiphilium rubrum sp. nov.: Acidophilic Heterotrophic Bacteria Isolated from Acidic Coal Mine Drainage. International Journal of Systematic and Evolutionary Microbiology, 36, 197-201.
http://dx.doi.org/10.1099/00207713-36-2-197
[48] Nazaries, L., Murrell, J.C., Millard, P., Baggs, L. and Singh, B.K. (2013) Methane, Microbes and Models: Fundamental Understanding of the Soil Methane Cycle for Future Predictions. Environmental Microbiology, 15, 2395-2417.
http://dx.doi.org/10.1111/1462-2920.12149
[49] Vecherskaya, M., Dijkema, C., Saad, H.R. and Stams, A.J.M. (2009) Microaerobic and Anaerobic Metabolism of a Methylocystis parvus Strain Isolated from a Denitrifying Bioreactor. Environmental Microbiology Reports, 1, 442-449. http://dx.doi.org/10.1111/j.1758-2229.2009.00069.x
[50] Oude Elferink, S.J.W.H., Akkermans-Van Vliet, W.M., Bogte, J.J. and Stams, A.J.M. (1999) Desulfobacca acetoxidans gen. nov., sp. nov., a Novel Acetate-Degrading Sulfate Reducer Isolated from Sulfidogenic Granular Sludge. International Journal of Systematic Bacteriology, 49, 345-350.
[51] Mcinerney, M.J., Struchtemeyer, C.G., Sieber, J., Mouttaki, H., Stams, A.J., Schink, B., Rohlin, L. and Gunsalus, R.P. (2008) Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism. Annals of the New York Academy of Sciences, 1125, 58-72. http://dx.doi.org/10.1196/annals.1419.005
[52] Chauhan, A. and Ogram, A. (2006) Phylogeny of Acetate-Utilizing Microorganisms in Soils along a Nutrient Gradient in the Florida Everglades. Applied and Environmental Microbiology, 72, 6837-6840.
http://dx.doi.org/10.1128/AEM.01030-06
[53] Puglisi, E., Zaccone, C., Cappa, F., Cocconcelli, P.S., Shotyk, W., Trevisan, M. and Miano, T.M. (2014) Changes in Bacterial and Archaeal Community Assemblages along an Ombrotrophic Peat Bog Profile. Biology and Fertility of Soils, 50, 815-826.
[54] Stoecker, K., Bendinger, B., Schoning, B., Nielsen, P.H., Nielsen, J.L., Baranyi, C., Toenshoff, E.R., Daims, H. and Wagner, M. (2006) Cohn’s Crenothrix Is a Filamentous Methane Oxidizer with an Unusual Methane Monooxygenase. Proceedings of the National Academy of Sciences of the United States of America, 103, 2363-2367.
http://dx.doi.org/10.1073/pnas.0506361103
[55] Kalyuzhnaya, M.G., Yang, S., Rozova, O.N., Smalley, N.E., Clubb, J., Lamb, A., Nagana Gowda, G.A., Raftery, D., Fu, Y., Bringel, F., Vuilleumier, S., Beck, D.A.C., Trotsenko, Y.A., Khmelenina, V.N. and Lidstrom, M.E. (2013) Highly Efficient Methane Biocatalysis Revealed in a Methanotrophic Bacterium. Nature Communications, 4, No. 2785. http://dx.doi.org/10.1038/ncomms3785
[56] Alfreider, A., Vogt, C. and Babel, W. (2002) Microbial Diversity in an in Situ Reactor System Treating Monochlorobenzene Contaminated Groundwater as Revealed by 16S Ribosomal DNA Analysis. Systematic and Applied Microbiology, 25, 232-240. http://dx.doi.org/10.1078/0723-2020-00111
[57] Hug, L.A., Castelle, C.J., Wrighton, K.C., Thomas, B.C., Sharon, I., Frischkorn, K.R., Banfield, J.F., et al. (2013) Community Genomic Analyses Constrain the Distribution of Metabolic Traits across the Chloroflexi Phylum and Indicate Roles in Sediment Carbon Cycling. Microbiome, 1, 22.
http://dx.doi.org/10.1186/2049-2618-1-22
[58] Loffler, F.E., Yan, J., Ritalahti, K.M., Adrian, L., Edwards, E.A., Konstantinidis, K.T., Müller, J.A., Fullerton, H., Zinder, S.H. and Spormann, A.M. (2013) Dehalococcoides mccartyi gen. nov., sp. nov., Obligately Organohalide-Respiring Anaerobic Bacteria Relevant to Halogen Cycling and Bioremediation, Belong to a Novel Bacterial Class, Dehalococcoidia Classis nov., Order Dehalococcoidales ord. nov. and Family Dehalococcoidaceae fam. nov., within the Phylum Chloroflexi. International Journal of Systematic and Evolutionary Microbiology, 63, 625-635.
http://dx.doi.org/10.1099/ijs.0.034926-0
[59] Biester, H., Martinez Cortizas, A. and Keppler, F. (2006) Occurrence and Fate of Halogens in Mires. In: Martini, I.P., Cortizas, A.M. and Chesworth, W., Eds., Peatlands: Evolution and Records of Environmental and Climate Changes, Elsevier Series Development in Earth Surface Processes, Vol. 9, Elsevier, Amsterdam, 449-465.
[60] Blazejak, A. and Schippers, A. (2010) High Abundance of JS-1-and Chloroflexi-Related Bacteria in Deeply Buried Marine Sediments Revealed by Quantitative, Real-Time PCR. FEMS Microbiology Ecology, 72, 198-207.
http://dx.doi.org/10.1111/j.1574-6941.2010.00838.x
[61] Yamada, T., Sekiguchi, Y., Imachi, H., Kamagata, Y., Ohashi, A. and Harada, H. (2005) Diversity, Localization, and Physiological Properties of Filamentous Microbes Belonging to Chloroflexi Subphylum I in Mesophilic and Thermophilic Methanogenic Sludge Granules. Applied and Environmental Microbiology, 71, 7493-7503.
http://dx.doi.org/10.1128/AEM.71.11.7493-7503.2005
[62] Wang, Y., Sheng, H.F., He, Y., Wu, J.Y., Jiang, Y.X., Tam, N.F.Y. and Zhou, H.W. (2012) Comparison of the Levels of Bacterial Diversity in Freshwater, Intertidal Wetland, and Marine Sediments by Using Millions of Illumina Tags. Applied and Environmental Microbiology, 78, 8264-8271.
http://dx.doi.org/10.1128/AEM.01821-12
[63] Sekiguchi, Y., Yamada, T., Hanada, S., Ohashi, A., Harada, H. and Kamagata, Y. (2003) Anaerolinea thermophila gen. nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., Novel Filamentous Thermophiles that Represent a Previously Uncultured Lineage of the Domain Bacteria at the Subphylum Level. International Journal of Systematic and Evolutionary Microbiology, 53, 1843-1851.
http://dx.doi.org/10.1099/ijs.0.02699-0
[64] Lienen, T., Kleybocker, A., Brehmer, M., Kraume, M., Moeller, L., G?rsch, K. and Würdemann, H. (2013) Floating Layer Formation, Foaming, and Microbial Community Structure Change in Full-Scale Biogas Plant Due to Disruption of Mixing and Substrate Overloading. Energy, Sustainability and Society, 3, 20.
http://dx.doi.org/10.1186/2192-0567-3-20
[65] Huang, X.F., Liu, Y.J., Dong, J.D., Qu, L.Y., Zhang, Y.Y., Wang, F.Z., Tian, X.P. and Zhang, S. (2014) Mangrovibacterium diazotrophicum gen. nov., sp. nov., a Nitrogen-Fixing Bacterium Isolated from a Mangrove Sediment, and Proposal of Prolixibacteraceae fam. nov. International Journal of Systematic and Evolutionary Microbiology, 64, 875-881. http://dx.doi.org/10.1099/ijs.0.052779-0
[66] Van Passel, M.W., Kant, R., Palva, A., Copeland, A., Lucas, S., Lapidus, A., Smidt, H., et al. (2011) Genome Sequence of the Verrucomicrobium Opitutus terrae PB90-1, an Abundant Inhabitant of Rice Paddy Soil Ecosystems. Journal of Bacteriology, 193, 2367-2368. http://dx.doi.org/10.1128/JB.00228-11
[67] Isanapong, J., Goodwin, L., Bruce, D., Chen, A., Detter, C., Han, J., Rodrigues, J.L., et al. (2012) High-Quality Draft Genome Sequence of the Opitutaceae Bacterium Strain TAV1, a Symbiont of the Wood-Feeding Termite Reticulitermes flavipes. Journal of Bacteriology, 194, 2744-2745. http://dx.doi.org/10.1128/JB.00264-12
[68] Sangwan, P., Kovac, S., Davis, K.E., Sait, M. and Janssen, P.H. (2005) Detection and Cultivation of Soil Verrucomicrobia. Applied and Environmental Microbiology, 71, 8402-8410.
http://dx.doi.org/10.1128/AEM.71.12.8402-8410.2005
[69] Khadem, A.F., Pol, A., Wieczorek, A., Mohammadi, S.S., Francoijs, K.J., Stunnenberg, H.G., Jetten, M. and Op den Camp, H.J.M. (2011) Autotrophic Methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicum solv Uses the Calvin-Benson-Bassham Cycle for Carbon Dioxide Fixation. Journal of Bacteriology, 193, 4438-4446.
http://dx.doi.org/10.1128/JB.00407-11
[70] Fukunaga, Y., Kurahashi, M., Sakiyama, Y., Ohuchi, M., Yokota, A. and Harayama, S. (2009) Phycisphaera mikurensis gen. nov., sp. nov., Isolated from a Marine Alga, and Proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae Classis nov. in the Phylum Planctomycetes. Journal of General and Applied Mirobiology, 55, 267-275. http://dx.doi.org/10.2323/jgam.55.267
[71] Kulichevskaya, I.S., Baulina, O.I., Bodelier, P.L.E., Rijpstra, W.I.C., Damsté, J.S.S. and Dedysh, S.N. (2009) Zavarzinella formosa gen. nov., sp. nov., a Novel Stalked, Gemmata-Like Planctomycete from a Siberian Peat Bog. International Journal of Systematic and Evolutionary Microbiology, 59, 357-364. http://dx.doi.org/10.1099/ijs.0.002378-0
[72] Kulichevskaya, I.S., Serkebaeva, Y.M., Kim, Y., Rijpstra, W.I.C., Damsté, J.S.S., Liesack, W. and Dedysh, S.N. (2012) Telmatocola sphagniphila gen. nov., sp. nov., a Novel Dendriform Planctomycete from Northern Wetlands. Frontiers in Microbiology, 3, 146. http://dx.doi.org/10.3389/fmicb.2012.00146
[73] Yoon, J., Jang, J.H. and Kasai, H. (2014) Algisphaera agarilytica gen. nov., sp. nov., a Novel Representative of the Class Phycisphaerae within the Phylum Planctomycetes Isolated from a Marine Alga. Antonie van Leeuwenhoek, 105, 317-324. http://dx.doi.org/10.1007/s10482-013-0076-1
[74] Ivanova, A.O. and Dedysh, S.N. (2012) Abundance, Diversity and Depth Distribution of Planctomycetes in Acidic Northern Wetlands. Frontiers in Microbiology, 3, 5. http://dx.doi.org/10.3389/fmicb.2012.00005
[75] Strous, M., Fuerst, J.A., Kramer, E.H., Logemann, S., Muyzer, G., Van De Pas-Schoonen, K.T., Webb, R., Kuenen, J.G. and Jetten, M.S. (1999) Missing Lithotroph Identified as New Planctomycete. Nature, 400, 446-449.
http://dx.doi.org/10.1038/22749
[76] Bragina, A., Maier, S., Berg, C., Müller, H., Chobot, V., Hadacek, F. and Berg, G. (2011) Similar Diversity of Alphaproteobacteria and Nitrogenase Gene Amplicons on Two Related Sphagnum Mosses. Frontiers in Microbiology, 2, 275.
[77] Hugenholtz, P., Pitulle, C., Hershberger, K.L. and Pace, N.R. (1998) Novel Division Level Bacterial Diversity in a Yellowstone Hot Spring. Journal of Bacteriology, 180, 366-376.
[78] Farag, I.F., Davis, J.P., Youssef, N.H. and Elshahed, M.S. (2014) Global Patterns of Abundance, Diversity and Community Structure of the Aminicenantes (Candidate Phylum OP8). PLoS ONE, 9, e92139.
http://dx.doi.org/10.1371/journal.pone.0092139
[79] Wu, M.L., Van Teeseling, M.C., Willems, M.J., Van Donselaar, E.G., Klingl, A., Rachel, R. and Van Niftrik, L. (2012) Ultrastructure of the Denitrifying Methanotroph “Candidatus Methylomirabilis Oxyfera,” a Novel Polygon-Shaped Bacterium. Journal of Bacteriology, 194, 284-291. http://dx.doi.org/10.1128/JB.05816-11
[80] Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M.M., Schreiber, F., Dutilh, B.E., Zedelius, J., De Beer, D., Gloerich, J., Wessels, H.J.C.T., Van Alen, T., Luesken, F., Wu, M.L., Van De Pas-Schoonen, K.T., Op Den Camp, H.J.M., Janssen-Megens, E.M., Francoijs, K.J., Stunnenberg, H., Weissenbach, J., Jetten, M.S.M. and Strous, M. (2010) Nitrite-Driven Anaerobic Methane Oxidation by Oxygenic Bacteria. Nature, 464, 543-548.
http://dx.doi.org/10.1038/nature08883

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.