The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing

Microbial-mat communities in the effluent channels of Octopus and Mushroom Springs within the Lower Geyser Basin at Yellowstone National Park have been studied for nearly 50 years. The emphasis has mostly focused on the chlorophototrophic bacterial organisms of the phyla Cyanobacteria and Chloroflexi. In contrast, the diversity and metabolic functions of the heterotrophic community in the microoxic/anoxic region of the mat are not well understood. In this study we analyzed the orange-colored undermat of the microbial community of Mushroom Spring using metagenomic and rRNA-amplicon (iTag) analyses. Our analyses disclosed a highly diverse community exhibiting a high degree of unevenness, strongly dominated by a single taxon, the filamentous anoxygenic phototroph, Roseiflexus spp. The second most abundant organisms belonged to the Thermotogae, which have been hypothesized to be a major source of H2 from fermentation that could enable photomixotrophic metabolism by Chloroflexus and Roseiflexus spp. Other abundant organisms include two members of the Armatimonadetes (OP10); Thermocrinis sp.; and phototrophic and heterotrophic members of the Chloroflexi. Further, an Atribacteria (OP9/JS1) member; a sulfate-reducing Thermodesulfovibrio sp.; a Planctomycetes member; a member of the EM3 group tentatively affiliated with the Thermotogae, as well as a putative member of the Arminicenantes (OP8) represented ≥1% of the reads. Archaea were not abundant in the iTag analysis, and no metagenomic bin representing an archaeon was identified. A high microdiversity of 16S rRNA gene sequences was identified for the dominant taxon, Roseiflexus spp. Previous studies demonstrated that highly similar Synechococcus variants in the upper layer of the mats represent ecological species populations with specific ecological adaptations. This study suggests that similar putative ecotypes specifically adapted to different niches occur within the undermat community, particularly for Roseiflexus spp.

[1]  D. M. Ward,et al.  A Panoply of Phototrophs: An Overview of the Thermophilic Chlorophototrophs of the Microbial Mats of Alkaline Siliceous Hot Springs in Yellowstone National Park, WY, USA , 2017 .

[2]  B. Simmons,et al.  Refining the phylum Chlorobi by resolving the phylogeny and metabolic potential of the representative of a deeply branching, uncultivated lineage , 2015, The ISME Journal.

[3]  D. M. Ward,et al.  The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light , 2015, Front. Microbiol..

[4]  Jason M. Wood,et al.  The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat , 2015, Front. Microbiol..

[5]  Jason M. Wood,et al.  The molecular dimension of microbial species: 1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park , 2015, Front. Microbiol..

[6]  S. Hallam,et al.  Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics , 2015, The ISME Journal.

[7]  D. Bryant,et al.  Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. , 2015, International journal of systematic and evolutionary microbiology.

[8]  Jason M. Wood,et al.  Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms , 2015, Front. Microbiol..

[9]  D. Bryant,et al.  Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum , 2015, Front. Microbiol..

[10]  D. M. Ward,et al.  Draft Genome Sequence of the Deinococcus-Thermus Bacterium Meiothermus ruber Strain A , 2015, Genome Announcements.

[11]  E. Bonch‐Osmolovskaya,et al.  Thermogutta terrifontis gen. nov., sp. nov. and Thermogutta hypogea sp. nov., thermophilic anaerobic representatives of the phylum Planctomycetes. , 2015, International journal of systematic and evolutionary microbiology.

[12]  F. Robb,et al.  Genome Sequence of the Sulfate-Reducing Thermophilic Bacterium Thermodesulfovibrio yellowstonii Strain DSM 11347T (Phylum Nitrospirae) , 2015, Genome Announcements.

[13]  Kwang-Hwan Jung,et al.  Cyanobacterial Light-Driven Proton Pump, Gloeobacter Rhodopsin: Complementarity between Rhodopsin-Based Energy Production and Photosynthesis , 2014, PloS one.

[14]  D. M. Ward,et al.  Draft Genome Sequence of a Sulfide-Oxidizing, Autotrophic Filamentous Anoxygenic Phototrophic Bacterium, Chloroflexus sp. Strain MS-G (Chloroflexi) , 2014, Genome Announcements.

[15]  L. Tomsho,et al.  Draft Genome Sequence of the Moderately Thermophilic Bacterium Schleiferia thermophila Strain Yellowstone (Bacteroidetes) , 2014, Genome Announcements.

[16]  N. Youssef,et al.  Global Patterns of Abundance, Diversity and Community Structure of the Aminicenantes (Candidate Phylum OP8) , 2014, PloS one.

[17]  Johan Hofkens,et al.  Super-resolution optical DNA Mapping via DNA methyltransferase-directed click chemistry , 2014, Nucleic acids research.

[18]  C. Kerepesi,et al.  AmphoraNet: the webserver implementation of the AMPHORA2 metagenomic workflow suite. , 2014, Gene.

[19]  Fangfang Xia,et al.  The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) , 2013, Nucleic Acids Res..

[20]  I-Min A. Chen,et al.  IMG/M 4 version of the integrated metagenome comparative analysis system , 2013, Nucleic Acids Res..

[21]  Y. Furushima,et al.  Isolation and Characterization of a Thermophilic, Obligately Anaerobic and Heterotrophic Marine Chloroflexi Bacterium from a Chloroflexi-dominated Microbial Community Associated with a Japanese Shallow Hydrothermal System, and Proposal for Thermomarinilinea lacunofontalis gen. nov., sp. nov. , 2013, Microbes and environments.

[22]  Christian A. Ross,et al.  Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage , 2013, Nature Communications.

[23]  Christian G. Klatt,et al.  Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring , 2013, The ISME Journal.

[24]  Martin Wu,et al.  Surprisingly extensive mixed phylogenetic and ecological signals among bacterial Operational Taxonomic Units , 2013, Nucleic acids research.

[25]  X. Morgan,et al.  Phylogenetic Delineation of the Novel Phylum Armatimonadetes (Former Candidate Division OP10) and Definition of Two Novel Candidate Divisions , 2013, Applied and Environmental Microbiology.

[26]  Markus J. Herrgård,et al.  Community Structure and Function of High-Temperature Chlorophototrophic Microbial Mats Inhabiting Diverse Geothermal Environments , 2013, Front. Microbiol..

[27]  N. Ravin,et al.  Genomic Analysis of Melioribacter roseus, Facultatively Anaerobic Organotrophic Bacterium Representing a Novel Deep Lineage within Bacteriodetes/Chlorobi Group , 2013, PloS one.

[28]  S. Rhee,et al.  Description of Fimbriimonas ginsengisoli gen. nov., sp. nov. within the Fimbriimonadia class nov., of the phylum Armatimonadetes , 2012, Antonie van Leeuwenhoek.

[29]  Christian G. Klatt,et al.  ‘Candidatus Thermochlorobacter aerophilum:’ an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics , 2012, The ISME Journal.

[30]  Stefan Schouten,et al.  Identification of the Bacteriochlorophylls, Carotenoids, Quinones, Lipids, and Hopanoids of “Candidatus Chloracidobacterium thermophilum” , 2011, Journal of bacteriology.

[31]  P. Bonin,et al.  Isolation and characterization of Thermanaerothrix daxensis gen. nov., sp. nov., a thermophilic anaerobic bacterium pertaining to the phylum "Chloroflexi", isolated from a deep hot aquifer in the Aquitaine Basin. , 2011, Systematic and applied microbiology.

[32]  X. Morgan,et al.  Chthonomonas calidirosea gen. nov., sp. nov., an aerobic, pigmented, thermophilic micro-organism of a novel bacterial class, Chthonomonadetes classis nov., of the newly described phylum Armatimonadetes originally designated candidate division OP10. , 2011, International journal of systematic and evolutionary microbiology.

[33]  C. Kuske,et al.  Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter usitatus Ellin6076 , 2011, PloS one.

[34]  D. M. Ward,et al.  Fine-Scale Distribution Patterns of Synechococcus Ecological Diversity in Microbial Mats of Mushroom Spring, Yellowstone National Park , 2011, Applied and Environmental Microbiology.

[35]  D. Meyer-dombard,et al.  Hydrothermal ecotones and streamer biofilm communities in the Lower Geyser Basin, Yellowstone National Park. , 2011, Environmental microbiology.

[36]  Christian G. Klatt,et al.  Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat , 2011, The ISME Journal.

[37]  Y. Kamagata,et al.  Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10. , 2011, International journal of systematic and evolutionary microbiology.

[38]  J. Bunge,et al.  Protistan microbial observatory in the Cariaco Basin, Caribbean. II. Habitat specialization , 2011, The ISME Journal.

[39]  D. Bhaya,et al.  In situ dynamics of O2, pH and cyanobacterial transcripts associated with CCM, photosynthesis and detoxification of ROS , 2011, The ISME Journal.

[40]  D. M. Ward,et al.  Influence of Molecular Resolution on Sequence-Based Discovery of Ecological Diversity among Synechococcus Populations in an Alkaline Siliceous Hot Spring Microbial Mat , 2010, Applied and Environmental Microbiology.

[41]  M. Hattori,et al.  Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group , 2010, Nucleic acids research.

[42]  S. Takaichi,et al.  Roseomonas aestuarii sp. nov., a bacteriochlorophyll-a containing alphaproteobacterium isolated from an estuarine habitat of India. , 2010, Systematic and applied microbiology.

[43]  S. Harayama,et al.  Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. , 2010, International journal of systematic and evolutionary microbiology.

[44]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[45]  Christian G. Klatt,et al.  Cultivation and Genomic, Nutritional, and Lipid Biomarker Characterization of Roseiflexus Strains Closely Related to Predominant In Situ Populations Inhabiting Yellowstone Hot Spring Microbial Mats , 2010, Journal of bacteriology.

[46]  Keita Yamada,et al.  Microbial methane production in deep aquifer associated with the accretionary prism in Southwest Japan , 2010, The ISME Journal.

[47]  N. Pace.  Mapping the Tree of Life: Progress and Prospects , 2009, Microbiology and Molecular Biology Reviews.

[48]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[49]  J. Banfield,et al.  Community-wide analysis of microbial genome sequence signatures , 2009, Genome Biology.

[50]  Patrick Wincker,et al.  Generation and analysis of a 29,745 unique Expressed Sequence Tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase , 2009, BMC Genomics.

[51]  F. Robb,et al.  Complete Genome Sequence of the Aerobic CO-Oxidizing Thermophile Thermomicrobium roseum , 2009, PloS one.

[52]  James R. Cole,et al.  The Ribosomal Database Project: improved alignments and new tools for rRNA analysis , 2008, Nucleic Acids Res..

[53]  Michael Kühl,et al.  Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat , 2008, The ISME Journal.

[54]  F. Rainey,et al.  Elioraea tepidiphila gen. nov., sp. nov., a slightly thermophilic member of the Alphaproteobacteria. , 2008, International journal of systematic and evolutionary microbiology.

[55]  M. Könneke,et al.  Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. , 2008, Environmental microbiology.

[56]  Rick L. Stevens,et al.  The RAST Server: Rapid Annotations using Subsystems Technology , 2008, BMC Genomics.

[57]  Natalia Khuri,et al.  Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses , 2007, The ISME Journal.

[58]  Christian G. Klatt,et al.  Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. , 2007, Environmental microbiology.

[59]  Donald A. Bryant,et al.  Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium , 2007, Science.

[60]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[61]  Scott R. Miller,et al.  High Rates of Sulfate Reduction in a Low-Sulfate Hot Spring Microbial Mat Are Driven by a Low Level of Diversity of Sulfate-Respiring Microorganisms , 2007, Applied and Environmental Microbiology.

[62]  F. Cohan,et al.  A Systematics for Discovering the Fundamental Units of Bacterial Diversity , 2007, Current Biology.

[63]  Patricia A. Hunt,et al.  The Mre11 Complex Influences DNA Repair, Synapsis, and Crossing Over in Murine Meiosis , 2007, Current Biology.

[64]  D. M. Ward,et al.  Impact of carbon metabolism on 13C signatures of cyanobacteria and green non-sulfur-like bacteria inhabiting a microbial mat from an alkaline siliceous hot spring in Yellowstone National Park (USA). , 2007, Environmental microbiology.

[65]  D. Bryant,et al.  Prokaryotic photosynthesis and phototrophy illuminated. , 2006, Trends in microbiology.

[66]  David M. Ward,et al.  Effect of Temperature and Light on Growth of and Photosynthesis by Synechococcus Isolates Typical of Those Predominating in the Octopus Spring Microbial Mat Community of Yellowstone National Park , 2006, Applied and Environmental Microbiology.

[67]  Michael C. Wendl,et al.  Argonaute—a database for gene regulation by mammalian microRNAs , 2005, BMC Bioinformatics.

[68]  Andrea Wieland,et al.  Diel Variations in Carbon Metabolism by Green Nonsulfur-Like Bacteria in Alkaline Siliceous Hot Spring Microbial Mats from Yellowstone National Park , 2005, Applied and Environmental Microbiology.

[69]  J. Handelsman,et al.  Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness , 2005, Applied and Environmental Microbiology.

[70]  K. Schleifer,et al.  ARB: a software environment for sequence data. , 2004, Nucleic acids research.

[71]  Hideki Harada,et al.  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. , 2003, International journal of systematic and evolutionary microbiology.

[72]  D. M. Ward,et al.  Compound-Specific Isotopic Fractionation Patterns Suggest Different Carbon Metabolisms among Chloroflexus-Like Bacteria in Hot-Spring Microbial Mats , 2003, Applied and Environmental Microbiology.

[73]  D. M. Ward,et al.  Cyanobacterial Ecotypes in Different Optical Microenvironments of a 68°C Hot Spring Mat Community Revealed by 16S-23S rRNA Internal Transcribed Spacer Region Variation , 2003, Applied and Environmental Microbiology.

[74]  D. M. Ward,et al.  Microscopic Examination of Distribution and Phenotypic Properties of Phylogenetically Diverse Chloroflexaceae-Related Bacteria in Hot Spring Microbial Mats , 2002, Applied and Environmental Microbiology.

[75]  R. Huber,et al.  New isolates and physiological properties of the Aquificales and description of Thermocrinis albus sp. nov. , 2002, Extremophiles.

[76]  B. Pierson,et al.  Molecular Characterization of Novel Red Green Nonsulfur Bacteria from Five Distinct Hot Spring Communities in Yellowstone National Park , 2002, Applied and Environmental Microbiology.

[77]  A. Reysenbach,et al.  Novel Bacterial and Archaeal Lineages from an In Situ Growth Chamber Deployed at a Mid-Atlantic Ridge Hydrothermal Vent , 2000, Applied and Environmental Microbiology.

[78]  R. Castenholz,et al.  Characterization of novel bacteriochlorophyll-a-containing red filaments from alkaline hot springs in Yellowstone National Park , 2000, Archives of Microbiology.

[79]  D. M. Ward,et al.  Highly Ordered Vertical Structure ofSynechococcus Populations within the One-Millimeter-Thick Photic Zone of a Hot Spring Cyanobacterial Mat , 2000, Applied and Environmental Microbiology.

[80]  David M. Ward,et al.  A Natural View of Microbial Biodiversity within Hot Spring Cyanobacterial Mat Communities , 1998, Microbiology and Molecular Biology Reviews.

[81]  R. Huber,et al.  Thermocrinis ruber gen. nov., sp. nov., a Pink-Filament-Forming Hyperthermophilic Bacterium Isolated from Yellowstone National Park , 1998, Applied and Environmental Microbiology.

[82]  Philip Hugenholtz,et al.  Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity , 1998, Journal of bacteriology.

[83]  D. M. Ward.  A natural species concept for prokaryotes. , 1998, Current opinion in microbiology.

[84]  N. Pace,et al.  Novel Division Level Bacterial Diversity in a Yellowstone Hot Spring , 1998, Journal of bacteriology.

[85]  B. Patel,et al.  Thermotoga hypogea sp. nov., a xylanolytic, thermophilic bacterium from an oil-producing well. , 1997, International journal of systematic bacteriology.

[86]  D. M. Ward,et al.  Population structure and physiological changes within a hot spring microbial mat community following disturbance , 1997, Applied and environmental microbiology.

[87]  D. M. Ward,et al.  Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis , 1997, Applied and environmental microbiology.

[88]  D. M. Ward,et al.  Biodiversity within hot spring microbial mat communities: molecular monitoring of enrichment cultures , 1997, Antonie van Leeuwenhoek.

[89]  D. M. Ward,et al.  Photosynthate partitioning and fermentation in hot spring microbial mat communities , 1996, Applied and environmental microbiology.

[90]  N. Pace,et al.  Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. , 1996, Trends in biotechnology.

[91]  D. M. Ward,et al.  Enrichment culture and microscopy conceal diverse thermophilic Synechococcus populations in a single hot spring microbial mat habitat , 1996, Applied and environmental microbiology.

[92]  D. M. Ward,et al.  Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community , 1996, Applied and environmental microbiology.

[93]  K. Schleifer,et al.  Phylogenetic identification and in situ detection of individual microbial cells without cultivation. , 1995, Microbiological reviews.

[94]  N. Pace,et al.  Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park , 1994, Applied and environmental microbiology.

[95]  D. M. Ward,et al.  Uncultivated cyanobacteria, Chloroflexus-like inhabitants, and spirochete-like inhabitants of a hot spring microbial mat , 1992, Applied and environmental microbiology.

[96]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[97]  H. Weiner,et al.  T-cell recognition of an immuno-dominant myelin basic protein epitope in multiple sclerosis , 1990, Nature.

[98]  D. M. Ward,et al.  16S rRNA sequences reveal numerous uncultured microorganisms in a natural community , 1990, Nature.

[99]  David M. Ward,et al.  Photoexcretion and Fate of Glycolate in a Hot Spring Cyanobacterial Mat , 1988, Applied and environmental microbiology.

[100]  David M. Ward,et al.  Formation and Fate of Fermentation Products in Hot Spring Cyanobacterial Mats , 1987, Applied and environmental microbiology.

[101]  D. M. Ward,et al.  Archaebacterial lipids in hot-spring microbial mats , 1985, Nature.

[102]  S. C. O'brien,et al.  C60: Buckminsterfullerene , 1985, Nature.

[103]  J. Lawton,et al.  Fractal dimension of vegetation and the distribution of arthropod body lengths , 1985, Nature.

[104]  D. M. Ward,et al.  Microelectrode Studies of Interstitial Water Chemistry and Photosynthetic Activity in a Hot Spring Microbial Mat , 1984, Applied and environmental microbiology.

[105]  D. M. Ward,et al.  Temperature Adaptations in the Terminal Processes of Anaerobic Decomposition of Yellowstone National Park and Icelandic Hot Spring Microbial Mats , 1982, Applied and environmental microbiology.

[106]  David M. Ward,et al.  Fate of Immediate Methane Precursors in Low-Sulfate, Hot-Spring Algal-Bacterial Mats , 1981, Applied and environmental microbiology.

[107]  D. M. Ward.  Thermophilic methanogenesis in a hot-spring algal-bacterial mat (71 to 30 degrees C) , 1978, Applied and environmental microbiology.

[108]  T. D. Brock,et al.  Structure, Growth, and Decomposition of Laminated Algal-Bacterial Mats in Alkaline Hot Springs , 1977, Applied and environmental microbiology.

[109]  T. D. Brock,et al.  Ecological studies of Chloroflexis, a gliding photosynthetic bacterium , 1973, Archiv für Mikrobiologie.

[110]  R. Castenholz.  Thermophilic Blue-Green Algae and the Thermal Environment , 1970, Bacteriological reviews.

[111]  H. Freeze,et al.  Thermus aquaticus gen. n. and sp. n., a Nonsporulating Extreme Thermophile , 1969, Journal of bacteriology.

[112]  T. D. Brock.  Micro-organisms adapted to High Temperatures , 1967, Nature.

[113]  Jason M. Wood,et al.  The molecular dimension of microbial species , 2018 .

[114]  Radhey S. Gupta,et al.  Erratum to: Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae , 2015, Antonie van Leeuwenhoek.

[115]  Deborah W. Gregory.  The Impact of Culture , 2014 .

[116]  Shane Nowack.  Niche character in a temporally varying environment , 2014 .

[117]  Radhey S. Gupta,et al.  Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) a , 2013, Antonie van Leeuwenhoek.

[118]  Radhey S. Gupta,et al.  Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov. , 2012, Antonie van Leeuwenhoek.

[119]  D. M. Ward,et al.  Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. , 2012, Environmental microbiology.

[120]  M. Lau,et al.  Bacterial community composition in thermophilic microbial mats from five hot springs in central Tibet , 2008, Extremophiles.

[121]  D. M. Ward,et al.  Microbial diversity in hot spring cyanobacterial mats: pattern and prediction , 2005 .

[122]  D. M. Ward,et al.  Community of Yellowstone National Park the Octopus Spring Microbial Mat Isolates Typical of Those Predominating in Synechococcus of and Photosynthesis by Effect of Temperature and Light on Growth , 2005 .

[123]  E. A. Henry,et al.  Characterization of a new thermophilic sulfate-reducing bacterium , 2004, Archives of Microbiology.

[124]  J. Degener,et al.  Denaturing gradient gel , 2003 .

[125]  Brian A. Whitton,et al.  The Ecology of Cyanobacteria , 2002, Springer Netherlands.

[126]  Scott R. Miller,et al.  Cyanobacteria in Geothermal Habitats , 2000 .

[127]  D. M. Ward,et al.  Ribosomal RNA Analysis of Microorganisms as They Occur in Nature , 1992 .

[128]  N. Pace,et al.  Microbial ecology and evolution: a ribosomal RNA approach. , 1986, Annual review of microbiology.

[129]  A. Chao.  Nonparametric estimation of the number of classes in a population , 1984 .

[130]  W. Meinschein,et al.  Thermomicrobium, a New Genus of Extremely Thermophilic Bacteria , 1973 .

[131]  M. Könneke,et al.  Cultivation of a Thermophilic Ammonia Oxidizing Archaeon Synthesizing Crenarchaeol , 2022 .

[132]  W. Moore,et al.  Taxonomic Note : A Place for DNA-DNA Reassociation and 16 s rRNA Sequence Analysis in the Present Species Definition in , 2022 .