Elioraea tepida, sp. nov., a Moderately Thermophilic Aerobic Anoxygenic Phototrophic Bacterium Isolated from the Mat Community of an Alkaline Siliceous Hot Spring in Yellowstone National Park, WY, USA

Saini, Mohit Kumar; Yoshida, Shohei; Sebastian, Aswathy; Hara, Eri; Tamaki, Hideyuki; Soulier, Nathan T.; Albert, Istvan; Hanada, Satoshi; Tank, Marcus; Bryant, Donald A.

doi:10.3390/microorganisms10010080

Title: Elioraea tepida, sp. nov., a Moderately Thermophilic Aerobic Anoxygenic Phototrophic Bacterium Isolated from the Mat Community of an Alkaline Siliceous Hot Spring in Yellowstone National Park, WY, USA

Journal Article · Fri Dec 31 00:00:00 EST 2021 · Microorganisms

DOI:https://doi.org/10.3390/microorganisms10010080· OSTI ID:1981165

^[1];

^[1]; Sebastian, Aswathy ^[2]; Hara, Eri ^[3]; Tamaki, Hideyuki ^[3]; Soulier, Nathan T. ^[2];

^[2]; Hanada, Satoshi ^[1]; Tank, Marcus ^[4];

^[2]

Tokyo Metropolitan University (Japan)
Pennsylvania State University, University Park, PA (United States)
National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba (Japan)
Tokyo Metropolitan University (Japan); Pennsylvania State University, University Park, PA (United States); DSMZ-German Culture Collection of Microorganisms and Cell Cultures, Braunschweig (Germany)

Strain MS-P2^T was isolated from microbial mats associated with Mushroom Spring, an alkaline siliceous hot spring in Yellowstone National Park, WY, USA. The isolate grows chemoheterotrophically by oxygen-dependent respiration, and light stimulates photoheterotrophic growth under strictly oxic conditions. Strain MS-P2^T synthesizes bacteriochlorophyll a and the carotenoid spirilloxanthin. However, photoautotrophic growth did not occur under oxic or anoxic conditions, suggesting that this strain should be classified as an aerobic anoxygenic phototrophic bacterium. Strain MS-P2^T cells are motile, curved rods about 0.5 to 1.0 μm wide and 1.0 to 1.5 μm long. The optimum growth temperature is 45–50 °C, and the optimum pH for growth is circum-neutral (pH 7.0–7.5). Sequence analysis of the 16S rRNA gene revealed that strain MS-P2^T is closely related to Elioraea species, members of the class Alphaproteobacteria, with a sequence identity of 96.58 to 98%. The genome of strain MS-P2^T is a single circular DNA molecule of 3,367,643 bp with a mol% guanine-plus-cytosine content of 70.6%. Based on phylogenetic, physiological, biochemical, and genomic characteristics, we propose this bacteriochlorophyll a-containing isolate is a new species belonging to the genus Elioraea, with the suggested name Elioraeatepida. The type-strain is strain MS-P2^T (= JCM33060^T = ATCC TSD-174^T).

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); Institute of Fermentation, Osaka (IFO); National Aeronautics and Space Administration (NASA); USDOE Office of Science (SC), Basic Energy Sciences (BES); Tokyo Metropolitan Government

Grant/Contract Number:: FG02-94ER20137; NNX16AJ62G

OSTI ID:: 1981165

Journal Information:: Microorganisms, Vol. 10, Issue 1; ISSN 2076-2607

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Porphyrobacter cryptus sp. nov., a novel slightly thermophilic, aerobic, bacteriochlorophyll a-containing species Rainey, F. A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1 https://doi.org/10.1099/ijs.0.02308-0	journal	January 2003
“Candidatus Thermonerobacter thiotrophicus,” A Non-phototrophic Member of the Bacteroidetes/Chlorobi With Dissimilatory Sulfur Metabolism in Hot Spring Mat Communities Thiel, Vera; Garcia Costas, Amaya M.; Fortney, Nathaniel W. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03159	journal	January 2019
Discovery of Natural Photosynthesis using Zn-Containing Bacteriochlorophyll in an Aerobic Bacterium Acidiphilium rubrum Wakao, N.; Yokoi, N.; Isoyama, N. Plant and Cell Physiology, Vol. 37, Issue 6 https://doi.org/10.1093/oxfordjournals.pcp.a029029	journal	September 1996
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium Tank, M.; Bryant, D. A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 5 https://doi.org/10.1099/ijs.0.000113	journal	February 2015
Analysis of 1,000+ Type-Strain Genomes Substantially Improves Taxonomic Classification of Alphaproteobacteria Hördt, Anton; López, Marina García; Meier-Kolthoff, Jan P. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00468	journal	April 2020
Biosynthesis of the modified tetrapyrroles—the pigments of life Bryant, Donald A.; Hunter, C. Neil; Warren, Martin J. Journal of Biological Chemistry, Vol. 295, Issue 20 https://doi.org/10.1074/jbc.REV120.006194	journal	April 2020
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences Kimura, Motoo Journal of Molecular Evolution, Vol. 16, Issue 2 https://doi.org/10.1007/BF01731581	journal	June 1980
Elioraea thermophila sp. nov., a thermophilic bacterium from hot spring of the class Alphaproteobacteria, emended description of the genus Elioraea and proposal of Elioraeaceae fam. nov. Habib, Neeli; Khan, Inam Ullah; Xiao, Min International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 2 https://doi.org/10.1099/ijsem.0.003915	journal	February 2020
‘Candidatus Thermochlorobacter aerophilum:’ an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics Liu, Zhenfeng; Klatt, Christian G.; Ludwig, Marcus The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.24	journal	March 2012
Porphyrobacter tepidarius sp. nov., a Moderately Thermophilic Aerobic Photosynthetic Bacterium Isolated from a Hot Spring Hanada, S.; Kawase, Y.; Hiraishi, A. International Journal of Systematic Bacteriology, Vol. 47, Issue 2 https://doi.org/10.1099/00207713-47-2-408	journal	April 1997
RefSeq: an update on prokaryotic genome annotation and curation Haft, Daniel H.; DiCuccio, Michael; Badretdin, Azat Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1068	journal	November 2017
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Genome sequence-based species delimitation with confidence intervals and improved distance functions Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-60	journal	January 2013
Rubritepida flocculans gen. nov., sp. nov., a New Slightly Thermophilic Member of the α-1 Subclass of the Proteobacteria Alarico, Susana; Rainey, Fred A.; Empadinhas, Nuno Systematic and Applied Microbiology, Vol. 25, Issue 2 https://doi.org/10.1078/0723-2020-00116	journal	January 2002
The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses Thiel, Vera; Hügler, Michael; Ward, David M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00943	journal	June 2017
Whole-Genome Sequence of a Unique Elioraea Species Strain Isolated from a Yellowstone National Park Hot Spring Robertson, Sydney; Ramaley, Robert F.; Meyer, Terry Microbiology Resource Announcements, Vol. 8, Issue 44 https://doi.org/10.1128/MRA.00907-19	journal	October 2019
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Notification of changes in taxonomic opinion previously published outside the IJSEM Oren, Aharon; Garrity, George International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 7 https://doi.org/10.1099/ijsem.0.004245	journal	July 2020
OrthoANI: An improved algorithm and software for calculating average nucleotide identity Lee, Imchang; Ouk Kim, Yeong; Park, Sang-Cheol International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 2 https://doi.org/10.1099/ijsem.0.000760	journal	February 2016
Genomic and Phenotypic Characterization of Chloracidobacterium Isolates Provides Evidence for Multiple Species Saini, Mohit Kumar; Sebastian, Aswathy; Shirotori, Yoshiki Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.704168	journal	June 2021
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Elioraea tepidiphila gen. nov., sp. nov., a slightly thermophilic member of the Alphaproteobacteria Albuquerque, L.; Rainey, F. A.; Nobre, M. F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 4 https://doi.org/10.1099/ijs.0.65294-0	journal	April 2008
Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. Keswani, J.; Whitman, W. B. International Journal of Systematic and Evolutionary Microbiology, Vol. 51, Issue 2 https://doi.org/10.1099/00207713-51-2-667	journal	March 2001
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 Thiel, Vera; Wood, Jason M.; Olsen, Millie T. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00919	journal	June 2016
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 Becraft, Eric D.; Wood, Jason M.; Rusch, Douglas B. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00590	journal	June 2015
Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses Bhaya, Devaki; Grossman, Arthur R.; Steunou, Anne-Soisig The ISME Journal, Vol. 1, Issue 8 https://doi.org/10.1038/ismej.2007.46	journal	October 2007
Humitalea rosea gen. nov., sp. nov., an aerobic bacteriochlorophyll-containing bacterium of the family Acetobacteraceae isolated from soil Margesin, R.; Zhang, D. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 4 https://doi.org/10.1099/ijs.0.043018-0	journal	July 2012
When should a DDH experiment be mandatory in microbial taxonomy? Meier-Kolthoff, Jan P.; Göker, Markus; Spröer, Cathrin Archives of Microbiology, Vol. 195, Issue 6 https://doi.org/10.1007/s00203-013-0888-4	journal	April 2013
Diversity of Chlorophototrophic Bacteria Revealed in the Omics Era Thiel, Vera; Tank, Marcus; Bryant, Donald A. Annual Review of Plant Biology, Vol. 69, Issue 1 https://doi.org/10.1146/annurev-arplant-042817-040500	journal	April 2018
RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation Li, Wenjun; O’Neill, Kathleen R.; Haft, Daniel H. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1105	journal	December 2020
Roseomonas aestuarii sp. nov., a bacteriochlorophyll-a containing alphaproteobacterium isolated from an estuarine habitat of India Venkata Ramana, V.; Sasikala, Ch; Takaichi, S. Systematic and Applied Microbiology, Vol. 33, Issue 4 https://doi.org/10.1016/j.syapm.2009.09.004	journal	June 2010
Ecology of aerobic anoxygenic phototrophs in aquatic environments Koblížek, Michal FEMS Microbiology Reviews, Vol. 39, Issue 6 https://doi.org/10.1093/femsre/fuv032	journal	July 2015
Phylogenetic Positions of Novel Aerobic, Bacteriochlorophyll a-Containing Bacteria and Description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. Yurkov, V.; Stackebrandt, E.; Holmes, A. International Journal of Systematic Bacteriology, Vol. 44, Issue 3 https://doi.org/10.1099/00207713-44-3-427	journal	July 1994
Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential Klatt, Christian G.; Wood, Jason M.; Rusch, Douglas B. The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.73	journal	June 2011
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes Brettin, Thomas; Davis, James J.; Disz, Terry Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08365	journal	February 2015
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum Tank, Marcus; Bryant, Donald A. Frontiers in Microbiology, Vol. 06 https://doi.org/10.3389/fmicb.2015.00226	journal	March 2015
Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring Klatt, Christian G.; Liu, Zhenfeng; Ludwig, Marcus The ISME Journal, Vol. 7, Issue 9 https://doi.org/10.1038/ismej.2013.52	journal	April 2013
TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy Meier-Kolthoff, Jan P.; Göker, Markus Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10210-3	journal	May 2019
Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat Liu, Zhenfeng; Klatt, Christian G.; Wood, Jason M. The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.37	journal	June 2011
Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Matsuura, Katsumi; Nakamura, Kazunori; Hanada, Satoshi International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 1 https://doi.org/10.1099/00207713-52-1-187	journal	January 2002
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1 https://doi.org/10.1139/y59-099	journal	January 1959
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
NCBI prokaryotic genome annotation pipeline Tatusova, Tatiana; DiCuccio, Michael; Badretdin, Azat Nucleic Acids Research, Vol. 44, Issue 14 https://doi.org/10.1093/nar/gkw569	journal	June 2016
Fatty Acid and Polar Lipid Composition in the Classification ofCellulomonas, Oerskoviaand Related Taxa Minnikin, D. E.; Collins, M. D.; Goodfellow, M. Journal of Applied Bacteriology, Vol. 47, Issue 1 https://doi.org/10.1111/j.1365-2672.1979.tb01172.x	journal	August 1979
Caldichromatium japonicum gen. nov., sp. nov., a novel thermophilic phototrophic purple sulphur bacterium of the Chromatiaceae isolated from Nakabusa hot springs, Japan Saini, Mohit Kumar; ChihChe, Weng; Soulier, Nathan International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 11 https://doi.org/10.1099/ijsem.0.004465	journal	November 2020
Genetic Manipulation of Carotenoid Biosynthesis in the Green Sulfur Bacterium Chlorobium tepidum Frigaard, N. -U.; Maresca, J. A.; Yunker, C. E. Journal of Bacteriology, Vol. 186, Issue 16 https://doi.org/10.1128/JB.186.16.5210-5220.2004	journal	August 2004
Proposal of Craurococcus roseus gen. nov., sp. nov. and Paracraurococcus ruber gen. nov., sp. nov., novel aerobic bacteriochlorophyll a-containing bacteria from soil Saitoh, S.; Suzuki, T.; Nishimura, Y. International Journal of Systematic Bacteriology, Vol. 48, Issue 3 https://doi.org/10.1099/00207713-48-3-1043	journal	July 1998
Elioraea rosea sp. nov., a plant promoting bacterium isolated from floodwater of a paddy field Lee, Hyo-Jin; Whang, Kyung-Sook International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 3 https://doi.org/10.1099/ijsem.0.004028	journal	March 2020
Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies Yoon, Seok-Hwan; Ha, Sung-Min; Kwon, Soonjae International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 5, p. 1613-1617 https://doi.org/10.1099/ijsem.0.001755	journal	May 2017

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59 BASIC BIOLOGICAL SCIENCES
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Title: Elioraea tepida, sp. nov., a Moderately Thermophilic Aerobic Anoxygenic Phototrophic Bacterium Isolated from the Mat Community of an Alkaline Siliceous Hot Spring in Yellowstone National Park, WY, USA

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