Skip to main content

Advertisement

SpringerLink
Log in

Complete genome of the thermophilic purple sulfur Bacterium Thermochromatium tepidum compared to Allochromatium vinosum and other Chromatiaceae

  • Original article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The complete genome sequence of the thermophilic purple sulfur bacterium Thermochromatium tepidum strain MCT (DSM 3771T) is described and contrasted with that of its mesophilic relative Allochromatium vinosum strain D (DSM 180T) and other Chromatiaceae. The Tch. tepidum genome is a single circular chromosome of 2,958,290 base pairs with no plasmids and is substantially smaller than the genome of Alc. vinosum. The Tch. tepidum genome encodes two forms of RuBisCO and contains nifHDK and several other genes encoding a molybdenum nitrogenase but lacks a gene encoding a protein that assembles the Fe–S cluster required to form a functional nitrogenase molybdenum-iron cofactor, leaving the phototroph phenotypically Nif–. Tch. tepidum contains genes necessary for oxidizing sulfide to sulfate as photosynthetic electron donor but is genetically unequipped to either oxidize thiosulfate as an electron donor or carry out assimilative sulfate reduction, both of which are physiological hallmarks of Alc. vinosum. Also unlike Alc. vinosum, Tch. tepidum is obligately phototrophic and unable to grow chemotrophically in darkness by respiration. Several genes present in the Alc. vinosum genome that are absent from the genome of Tch. tepidum likely contribute to the major physiological differences observed between these related purple sulfur bacteria that inhabit distinct ecological niches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The Tch. tepidum strain MCT (DSM 3771T; ATCC 43061T) whole genome shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession designation CP039268.1.

Abbreviations

Tch. :

Thermochromatium

Alc.:

Allochromatium

Ccm :

Caldichromatium

PSB:

Purple sulfur bacteria

References

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59:1525–1541

  • Baker JM, Riester CJ, Skinner BM, Newell AW, Swingley WD, Madigan MT, Jung DO, Asao M, Chen M, Loughlin PC, Pan H, Lin Y, Li Y, Shaw J, Prado M, Sherman C, Tang JK-H, Blankenship RE, Zhao T, Touchman JW, Sattley WM (2017) Genome sequence of Rhodoferax antarcticus ANT.BRT; a psychrophilic purple nonsulfur bacterium from an Antarctic microbial mat. Microorganisms 5:8. https://doi.org/10.3390/microorganisms501008

    Article  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boomer SM, Pierson BK, Austinhirst R, Castenhloz RW (2000) Characterization of novel bacteriochlorophyll-a-containing red filaments from alkaline hot springs in Yellowstone National Park. Arch Microbiol 174:152–161

    CAS  PubMed  Google Scholar 

  • Bowie JU (2005) Solving the membrane protein folding problem. Nature 438:581–589

    CAS  PubMed  Google Scholar 

  • Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365. https://doi.org/10.1038/srep08365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria, vol 2. Advances in Photosynthesis and Respiration. Kluwer Academic, Dordrecht, pp 847–870

    Google Scholar 

  • Carey A-M, Hacking K, Picken N, Honkanen S, Kelly S, Niedzwiedzki DM, Blankenship RE, Shimizu Y, Wang-Otomo Z-Y, Cogdell RJ (2014) Characterisation of the LH2 spectral variants produced by the photosynthetic purple sulphur bacterium Allochromatium vinosum. Biochim Biophys Acta 1837:1849–1860

    CAS  PubMed  Google Scholar 

  • Castenholz RW (1969) Thermophilic blue-green algae and the thermal environment. Bacteriol Rev 33:476–504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castenholz RW (1976) The effect of sulfide on the blue-green algae of hot springs. I. New Zealand and Iceland. J Phycol 12:54–68

    CAS  Google Scholar 

  • Castenholz RW (1977) The effect of sulfide on the blue-green algae of hot springs II. Yellowstone Park. Microb Ecol 3:79–105

    CAS  PubMed  Google Scholar 

  • Castenholz RW (2015) Portrait of a geothermal spring, Hunter’s Hot Springs, Oregon. Life 5:332–347

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castenholz RW, Pierson BK (1995) Ecology of thermophilic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 87–103

    Google Scholar 

  • Castillo MCG, Lou B-S, Ondrias MR, Robertson DE, Knaff DB (1994) Characterization of flavocytochrome c552 from the thermophilic photosynthetic bacterium Chromatium tepidum. Arch Biochem Biophys 315:262–266

    Google Scholar 

  • Chen J-H, Yu L-J, Boussac A, Wang-Otomo Z-Y, Kuang T, Shen J-R (2019) Properties and structure of a low-potential, penta-heme cytochrome c552 from a thermophilic purple sulfur photosynthetic bacterium Thermochromatium tepidum. Photosynth Res 139:281–293

    CAS  PubMed  Google Scholar 

  • Dahl C (2020) A biochemical view on the biological sulfur cycle. In: Lens PNL (ed) Environmental technologies to treat sulfur pollution: Principles and engineering, 2nd edn. IWA Publishing, London, pp 55–96

    Google Scholar 

  • Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R (2013) Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: Identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiology 159:2626–2638

    CAS  PubMed  Google Scholar 

  • Dahl C, Friedrich CG (eds) (2008) Microbial sulfur metabolism. Springer, Berlin, p 308

    Google Scholar 

  • Dewey ED, Stokes LM, Burchell BM et al (2020) Analysis of the complete genome of the alkaliphilic and phototrophic Firmicute Heliorestis convoluta strain HHT. Microorganisms 8:313. https://doi.org/10.3390/microorganisms8030313

    Article  CAS  PubMed Central  Google Scholar 

  • Dincturk HB, Demir V, Aykanat T (2011) Bd oxidase homologue of photosynthetic purple sulfur bacterium Allochromatium vinosum is co-transcribed with a nitrogen fixation related gene. Antonie Van Leeuwenhoek 99:211–220

    CAS  PubMed  Google Scholar 

  • Ehrenberg CG (1838) Monas okenii, Oken’s Stabmonade. Die Infusionsthierchen als vollkommene organismen ein blick in das tiefere organische leben der natur. Verlag von Leopold Voss, Leipzig, pp 15–16

    Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT et al (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci (USA) 99:9509–9514

    CAS  Google Scholar 

  • Fathir I, Ashikago M, Tanaka K, Katano T, Nirasawa T, Kobayashi M, Wang Z-Y, Nozawa T (1998) Biochemical and spectral characterization of the core light harvesting complex 1 (LH1) from the thermophilic purple sulfur bacterium Chromatium tepidum. Photosynth Res 58:193–202

    CAS  Google Scholar 

  • Fathir I, Tanaka K, Yoza K, Kojima A, Kobayashi M, Wang Z-Y, Lottspeich F, Nozawa T (1997) The genes coding for the L, M and cytochrome subunits of the photosynthetic reaction center from the thermophilic purple sulfur bacterium Chromatium tepidum. Photosynth Res 51:71–82

    CAS  Google Scholar 

  • Frigaard N-U, Bryant DA (2008) Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur Metabolism in phototrophic organisms, vol 27. Advances in Photosynthesis and Respiration. Heidelberg-Springer, pp 337–355

    Google Scholar 

  • Frigaard N-U, Dahl C (2009) Sulfur metabolism in phototrophic sulfur bacteria. In: Poole RK (ed) Advances in microbial physiology, vol 54. Academic Press, pp 103–200

    Google Scholar 

  • Fukuchi S, Nishikawa K (2001) Protein surface amino acid compositions distinctively differ between thermophilic and mesophilic bacteria. J Mol Biol 309:835–843

    CAS  PubMed  Google Scholar 

  • Garschagen LS, Franke T, Deppenmeier U (2020) An alternative pentose phosphate pathway in human gut bacteria for the degradation of C5 sugars in dietary fibers. FEBS J 288:1839–1858

    PubMed  Google Scholar 

  • Giovannoni SJ, Revsbech NP, Ward DM, Castenholz RW (1987) Obligately phototrophic Chloroflexus: primary production in anaerobic hot spring microbial mats. Arch Microbiol 147:80–87

    CAS  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    CAS  PubMed  Google Scholar 

  • Grimm F, Cort JR, Dahl C (2010) DsrA, a novel IscA-like protein lacking iron- and Fe-S-binding functions, involved in the regulation of sulfur oxidation in Allochromatium vinosum. J Bacteriol 192:1652–1661

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grimm F, Franz B, Dahl C (2011) Regulation of dissimilatory sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum. Front Microbiol 2:51

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heda GD, Madigan MT (1988) Thermal properties and oxygenase activity of ribulose 1,5-bisphosphate carboxylase from the thermophilic purple bacterium, Chromatium tepidum. FEMS Microbiol Letts 51:45–50

    CAS  Google Scholar 

  • Heda GD, Madigan MT (1989) Purification and characterization of ribulose-1,5-bisphosphate carboxylase from the thermophilic purple bacterium, Chromatium tepidum. Eur J Biochem 184:313–319

    CAS  PubMed  Google Scholar 

  • Hirano Y, Kimura Y, Suzuki H, Miki K, Wang ZY (2012) Structure analysis and comparative characterization of the cytochrome c´ and flavocytochrome c from thermophilic purple photosynthetic bacterium Thermochromatium tepidum. Biochemistry 51:6556–6567

    CAS  PubMed  Google Scholar 

  • Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) (2009) The purple phototrophic bacteria. Springer, Dordrecht

    Google Scholar 

  • Imhoff JF (2005) Genus II. Allochromatium. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2B. Springer, New York, pp 12–14

    Google Scholar 

  • Imhoff JF, Süling J, Petri R (1998) Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa and Thermochromatium. Int J Syst Bacteriol 48:1129–1143

    PubMed  Google Scholar 

  • Kämpf C, Pfennig N (1980) Capacity of Chromatiaceae for chemotrophic growth. Specific respiration rates of Thiocystis violacea and Chromatium vinosum. Arch Microbiol 127:125–135

    Google Scholar 

  • Karshikoff A, Landenstein R (2001) Ion pairs and the thermotolerance of proteins from hyperthermophiles: a “traffic rule” for hot roads. Trends Biochem Sci 26:550–556

    CAS  PubMed  Google Scholar 

  • Kawai S, Nishihara A, Matsuura K, Haruta S (2019) Hydrogen-dependent autotrophic growth in phototrophic and chemolithotrophic cultures of thermophilic bacteria, Chloroflexus aggregans and Chloroflexus aurantiacus, isolated from Nakabusa Hot springs. FEMS Letts. https://doi.org/10.1093/femsle/fnz122

    Article  Google Scholar 

  • Kawakami T, Yu LJ, Liang T, Okazaki K, Madigan MT, Kimura Y, Wang-Otomo ZY (2021) Crystal structure of a photosynthetic LH1-RC in complex with its electron donor HiPIP. Nat Commun 12:1104. https://doi.org/10.1038/s41467-021-21397-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy C, Dean D (1992) The nifU, nifS, and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinlandii. Molec Gen Genet 231:494–498

    CAS  PubMed  Google Scholar 

  • Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–341

    CAS  PubMed  Google Scholar 

  • Kimble LK, Mandelco L, Woese CR, Madigan MT (1995) Heliobacterium modesticaldum, sp.nov., a thermophilic heliobacterium of hot springs and volcanic soils. Arch Microbiol 163:259–267

    CAS  Google Scholar 

  • Kimura Y, Lyu S, Okoshi A, Okazaki K, Nakamura N, Ohashi A, Ohno T, Kobayashi M, Imanishi M, Takaichi S, Madigan MT, Wang-Otomo Z-Y (2017) Effects of calcum ions on the thermostability and spectroscopic properties of the LH1-RC complex from a new thermophilic purple bacterium Allochromatium tepidum. J Phys Chem B 21:5025–5032

    Google Scholar 

  • Kimura Y, Yu LJ, Hirano Y, Suzuki H, Wang ZY (2009) Calcium Ions Are required for the enhanced thermal stability of the light-harvesting-reaction center core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum. J Biol Chem 284:93–99

    CAS  PubMed  Google Scholar 

  • Kobayashi M, Saito T, Takahashi K, Wang Z-Y, Nozawa T (2005) Electronic properties and thermal stability of soluble redox proteins from a thermophilic purple sulfur photosynthetic bacterium, Thermochromatium tepidum. Bull Chem Soc Jpn 78:2164–2170

    CAS  Google Scholar 

  • Koendjbiharie JG, Hon S, Pabst M, Hooftman R, Stevenson DM, Cui J, Amador-Noguez D, Lynd LR, Olson DG, van Kranenburg, (2020) The pentose phosphate pathway of cellulolytic clostridia relies on 6-phosphofructokinase instead of transaldolase. J Biol Chem 295:1867–1878

    CAS  PubMed  Google Scholar 

  • Kumar S, Stetcher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 30:1870–1874

    Google Scholar 

  • Lefort V, Desper R, Gascuel O (2015) FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Nogi T, Kobayashi M, Nozawa T, Miki K (2002) Ultrahigh-resolution structure of high-potential iron-sulfur protein from Thermochromatium tepidum. Acta Crystallogr D 58:1085–1091

    PubMed  Google Scholar 

  • Löffler M, Feldhues J, Venceslau SS, Kammler L, Grein F, Pereira IAC, Dahl C (2020) DsrL mediates electron transfer between NADH and rDsrAB in Allochromatium vinosum. Environ Microbiol 22:783–795

    PubMed  Google Scholar 

  • Long M, Liu J, Chen Z, Bleijlevens B, Roseboom W, Albract SP (2007) Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module. J Biol Inorg Chem 12:62–78

    CAS  PubMed  Google Scholar 

  • Luedin SM, Liechti N, Cox RP, Danza F, Frigaard N-U, Posth NR, Pothier JF, Roman S, Storelli N, Wittwer M, Tonolla M (2019) Draft genome sequence of Chromatium okenii isolated from the stratified alpine Lake Cadagno. Sci Rep. https://doi.org/10.1038/s41598-018-38202-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma F, Yu LJ, Wang-Otomo ZY, van Grondelle R (2016) Temperature dependent LH1→ RC energy transfer in purple bacteria Tch. tepidum with shiftable LH1-Qy band: A natural system to investigate thermally activated energy transfer in photosynthesis. Biochim Biophys Acta 1857:408–414

    CAS  PubMed  Google Scholar 

  • MacKenzie KR, Engelman DM (1998) Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A dimerization. Proc Natl Acad Sci USA 95:3583–3590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Madigan MT (1984) A novel photosynthetic bacterium isolated from a Yellowstone hot spring. Science 225:313–315

    CAS  PubMed  Google Scholar 

  • Madigan MT (1986) Chromatium tepidum sp. nov., a thermophilic photosynthetic bacterium of the family Chromatiaceae. Intl J Syst Bacteriol 36:222–227

    CAS  Google Scholar 

  • Madigan MT, Takaigiku R, Lee RG, Gest H, Hayes JM (1989) Carbon isotopic fractionation by thermophilic phototrophic sulfur bacteria; evidence for autotrophic growth in natural populations. Appl Environ Microbiol 55:639–644

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maróti J, Farkas A, Ildikó KN, Maróti G, Kondorosi E, Rákhely G, Kovács KL (2010) A second soluble Hox-type NiFe enzyme completes the hydrogenase set in Thiocapsa roseopersicina BBS. Appl Environ Microbiol 76:5113–5123

    PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60

    Google Scholar 

  • Meruelo AD, Han SK, Kim S, Bowie JU (2012) Structural differences between thermophilic and mesophilic membrane proteins. Protein Sci 21:1746–1753

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miyoshi M (1897) Studien über die Schwefelrasenbildung und die Schwefelbakteriein der Thermen von Yumoto bei Nikko. Centralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 2:526–527

    Google Scholar 

  • Mouncey NJ, Choudhary M, Kaplan S (1997) Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: an essential metabolic gene function encoded on chromosome II. J Bacteriol 179:7617–7624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moulis JM, Scherrer N, Gagnon J, Forest E, Petillot Y, Garcia D (1993) Primary structure of Chromatium tepidum high-potential iron-sulfur protein in relation to thermal denaturation. Arch Biochem Biophys 305:186–192

    CAS  PubMed  Google Scholar 

  • Nagashima KVP et al (2017) Probing structure–function relationships in early events in photosynthesis using a chimeric photocomplex. Proc Natl Acad Sci USA 114:10906–10911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nagashima S, Nagashima KVP (2013) Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. In: Beatty JT (ed) Advances in Botanical Research: Genome evolution of photosynthetic bacteria. Academic Press, San Diego, pp 151–178

    Google Scholar 

  • Nagashima S, Shimada K, Matsuura K, Nagashima KVP (2002) Transcription of three sets of genes coding for the core light-harvesting proteins in the purple sulfur bacterium, Allochromatium vinosum. Photosynth Res 74:269–280

    CAS  PubMed  Google Scholar 

  • Nagatsuma S, Gotou K, Yamashita T, Yu L-J, Shen J-R, Madigan MT, Kimura Y, Wang-Otomo Z-Y (2019) Phospholipid distributions in purple phototrophic bacteria and LH1-RC core complexes. Biochim Biophys Acta-Bioenergetics 1860:461–468

    CAS  Google Scholar 

  • Niwa S et al (2014) Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å. Nature 508:228–232

    CAS  PubMed  Google Scholar 

  • Nogi T, Fathir I, Kobayashi M, Nozawa T, Miki K (2000) Crystal structures of photosynthetic reaction center and high-potential iron-sulfur protein from Thermochromatium tepidum: Thermostability and electron transfer. Proc Natl Acad Sci USA 97:13561–13566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nozawa TT, Fukada M, Hatano M, Madigan MT (1986) Organization of intracytoplasmic membranes in a novel thermophilic purple photosynthetic bacterium as revealed from absorption, circular dichroism, and emission spectra. Biochim Biophys Acta 852:191–197

    CAS  Google Scholar 

  • Otaki H, Everroad RC, Matsurau K, Hruta S (2012) Production and consumption of hydrogen in hot spring microbial mats dominated by a filamentous anoxygenic photosynthetic bacterium. Microbes Environ 27:293–299

    PubMed  PubMed Central  Google Scholar 

  • Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the rapid annotation of microbial genomes using subsystem technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226

    Article  CAS  PubMed  Google Scholar 

  • Perty M (1852) Zur Kenntnis kleinstr Lebensforman nack Bau, Funktionen, Systematik, mit Specialverzeichniss der in der Schweiz beobacteten. Verlag von Jent and Reinert, Bern , pp 1–228

    Google Scholar 

  • Pfennig N (1967) Photosynthetic bacteria. Ann Rev Microbiol 21:285–324

    CAS  Google Scholar 

  • Reinartz M, Tschäpe J, Brüser T, Trüper HG, Dahl C (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170:59–68

    CAS  PubMed  Google Scholar 

  • Roelofsen PA (1935). On photosynthesis of the Thiorhodaceae. Ph.D. dissertation. Rijksuniversiteit, Utrecht, Holland

  • Saini MK, ChihChe W, Soulier N, Sebastian A, Albert I, Thiel V, Bryant DA, Hanada S, Tank M (2020) Caldichromatium japonicum gen nov, sp nov, a novel thermophilic phototrophic purple sulphur bacterium of the Chromatiaceae isolated from Nakabusa hot springs. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.004465

    Article  PubMed  Google Scholar 

  • Sander J, Engels-Schwarzlose S, Dahl C (2006) Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186:357–366

    CAS  PubMed  Google Scholar 

  • Sattley WM, Madigan MT, Swingley WD et al (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190:4687–4696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sattley WM, Swingley WD (2013) Properties and evolutionary implications of the heliobacterial genome. In: Beatty JT (ed) Advances in Botanical Research: Genome Evolution of Photosynthetic Bacteria. Academic Press, San Diego, pp 151–178

    Google Scholar 

  • Schlegel HG, Pfennig N (1960) Die anreicherungskultur einiger schwefel- purpurbakterien. Arch Mikrobiol 38:1–39

    Google Scholar 

  • Sekine F, Horiguch K, Kashino Y, Shimizu Y, Yu L-J, Kobayashi M, Wang Z-Y (2012) Gene sequencing and characterization of the light-harvesting complex 2 from thermophilic purple sulfur bacterium Thermochromatium tepidum. Photosynth Res 111:9–18

    CAS  PubMed  Google Scholar 

  • Spatzal T, Schlesier J, Burger E-M, Sippel D, Zhang L, Andrade SLA, Rees DC, Einsle O (2016) Nitrogenase FeMoco investigated by spatially resolved anomalous dispersion refinement. Nat Commun 7:10902

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 131:1–32

    CAS  PubMed  Google Scholar 

  • Suzuki H, Hirano Y, Kimura Y, Takaichi S, Kobayashi M, Miki K, Wang Z-Y (2007) Purification, characterization and crystallization of the core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum. Biochim Biophys Acta 1767:1057–1063

    CAS  PubMed  Google Scholar 

  • Szilágyi A, Závodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8:493–504

    PubMed  Google Scholar 

  • Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S (2007) Function, structure, and evolution of the RubisCO-like proteins and their RuBisCO homologs. Microbiol Mol Biol Rev 71:576–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thiel V, Tank M, Bryant DA (2018) Diversity of chlorophototrophic bacteria revealed in the omics era. Ann Rev Plant Biol 69:21–49

    CAS  Google Scholar 

  • Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    CAS  PubMed  Google Scholar 

  • Wahlund TM, Woese CR, Castenholz RW, Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90

    CAS  Google Scholar 

  • Wahlund TM, Madigan MT (1995) Nitrogen fixation by the thermophilic green sulfur bacterium Chlorobium tepidum. J Bacteriol 175:474–478

    Google Scholar 

  • Wang Z-Y, Shimonaga M, Suzuki H, Kobayashi M, Nozawa T (2003) Purification and characterization of the polypeptides of core light-harvesting complexes from purple sulfur bacteria. Photosynth Res 78:133–141

    CAS  PubMed  Google Scholar 

  • Weissgerber T, Zigann R, Bruce D, Chang Y-J, Detter JC, Han C, Hauser L, Jeffries CD, Land M, Munk AC, Tapia R, Dahl C (2011) Complete genome sequence of Allochromatium vinosum DSM 180T. Stand Genomic Sci 5:311–330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Zhang Y, Guo X, Ren S, Staempfli AA, Chiao J, Jiang W, Zhao G (2004) Isoleucine biosynthesis in Leptospira interrogans lai strain 56601 via a threonine-independent pathway. J Bacteriol 186:5400–5409

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L-J, Suga M, Wang-Otomo Z-Y, Shen J-R (2018a) Novel features of LH1-RC from Thermochromatium tepidum revealed from its atomic resolution structure. FEBS J 285:4359–4366

    CAS  PubMed  Google Scholar 

  • Yu L-J, Suga M, Wang-Otomo Z-Y, Shen J-R (2018b) Structure of photosynthetic LH1-RC supercomplex at 1.9Å resolution. Nature 556:209–213

    CAS  PubMed  Google Scholar 

  • Zhang L, Jiang W, Nan J, Almqvist J, Huang Y (2014) The Escherichia coli CysZ is a pH dependent sulfate transporter that can be inhibited by sulfite. Biochim Biophys Acta 1838:1809–1816

    CAS  PubMed  Google Scholar 

  • Zhao D, Curatti L, Rubio LM (2007) Evidence for nifU and nifS participation in the biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Biol Chem 282:37016–37025

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

MTM thanks the United States National Park Service for the collection permit that allowed sampling in the Mammoth Hot Springs area in 1982 and the gracious hospitality of Dr. Dave Ward and the staff of his laboratory at Montana State University where Thermochromatium tepidum strain MCT was originally enriched. MTM also thanks the Bayerische Staatsbibliothek, Munich for a copy of the paper by Perty and Prof. Dr. Bernhard Schink, Konstanz for translation of the papers by Ehrenberg and Perty. We thank Kaelyn Nannini for assistance with ANI calculations and the Hodson Research Institute (Indiana Wesleyan University) for research grants supporting the participation of BMB, EDD, MKH, TLR, KNS, LMS, and WMS in this research.

Funding

This work was supported by the U.S. National Science Foundation Grant #0950550 to JWT, MTM, and REB. In addition, MTM received partial support from NASA Exobiology Grant NNX15AM17G.

Author information

Authors and Affiliations

  1. Division of Natural Sciences, Indiana Wesleyan University, Marion, IN, 46953, USA

    W. Matthew Sattley, Brad M. Burchell, Emma D. Dewey, Mackenzie K. Hayward, Tara L. Renbarger, Kathryn N. Shaffer & Lynn M. Stokes

  2. Department of Biological Sciences, Northern Illinois University, Dekalb, IL, 60115, USA

    Wesley D. Swingley, Sonja A. Gurbani, Catrina M. Kujawa, D. Adam Nuccio & Jacob Schladweiler

  3. School of Life Sciences, Arizona State University, Tempe, AR, 85287, USA

    Jeffrey W. Touchman

  4. Faculty of Science, Ibaraki University, Mito, Japan

    Zheng-Yu Wang-Otomo

  5. Departments of Chemistry and Biology, Washington University, St. Louis, MO, 63130, USA

    Robert E. Blankenship

  6. Department of Microbiology, School of Biological Sciences, Southern Illinois University, Carbondale, IL, 62901, USA

    Michael T. Madigan

Authors
  1. W. Matthew Sattley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wesley D. Swingley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brad M. Burchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emma D. Dewey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mackenzie K. Hayward
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tara L. Renbarger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kathryn N. Shaffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lynn M. Stokes
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sonja A. Gurbani
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Catrina M. Kujawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. D. Adam Nuccio
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jacob Schladweiler
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jeffrey W. Touchman
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Zheng-Yu Wang-Otomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Robert E. Blankenship
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Michael T. Madigan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JWT, MTM, REB, WDS, and WMS conceived and designed the experiments. MTM provided the culture of Tch. tepidum strain MCT. WMS, MTM, BMB, KNS, LMS, EDD, MKH, TLR, WDS, SAG, CMK, DAN, JS, and Z-YW-O performed comparative sequence analyses and analyzed the data. WDS coordinated submission and accessioning of the Tch. tepidum str. MCT genome sequence with GenBank. MTM, WMS, and EDD prepared the manuscript text, with WMS, MTM, Z-YW-O, MKH, LMS, EDD, and TLR providing tables and figures. All authors reviewed and finalized the submitted version of the paper.

Corresponding author

Correspondence to W. Matthew Sattley.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest relevant to the content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sattley, W.M., Swingley, W.D., Burchell, B.M. et al. Complete genome of the thermophilic purple sulfur Bacterium Thermochromatium tepidum compared to Allochromatium vinosum and other Chromatiaceae. Photosynth Res 151, 125–142 (2022). https://doi.org/10.1007/s11120-021-00870-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-021-00870-y

Keywords

Search

Navigation