Thermomicrobia
Scientific classification Edit this classification
Domain: Bacteria
Phylum: Thermomicrobiota
Garrity and Holt 2021[1]
Class: Thermomicrobia
Garrity and & Holt 2002[2]
Orders
Synonyms
  • Thermomicrobia:
    • "Thermomicrobia" Garrity and Holt 2001
    • "Thermomicrobiota" Whitman et al. 2018
    • "Thermomicrobaeota" Oren et al. 2015

The Thermomicrobia is a group of thermophilic green non-sulfur bacteria. Based on species Thermomicrobium roseum (type species) and Sphaerobacter thermophilus, this bacteria class has the following description:[3][4]

The class Thermomicrobia subdivides into two orders with validly published names: Thermomicrobiales Garrity and Holt 2001 and Sphaerobacterales Stackebrandt, Rainey and Ward-Rainey 1997. Gram negative. Pleomorphic, non-motile, non-spore-forming rods. Non-sporulating. No diamino acid present. No peptidoglycan in significant amount. Atypical proteinaceous cell walls. Hyper-thermophilic, optimum growth temperature at 70-75 °C. Obligatory aerobic and chemoorganotrophic. [note 1]

As thermophilic bacteria, members of this class are usually found in environments which are distant from human activity.[5] However, they have features like improved growth in antibiotics and CO oxidizing activity, making them interesting topics of research (e.g. for biotechnology application).

History

In 1973, a strain of rose-pink thermophilic bacteria was isolated from Toadstool Spring in Yellowstone National Park, which was later named Thermomicrobium roseum and proposed as a novel species of the novel genus Thermomicrobium.[6] At that time the genus was categorized under family Achromobacteraceae, but it became a distinct phylum by 2001.[3]

In 2004, it was proposed, on the basis of an analysis of genetic affiliations, that the Thermomicrobia should more properly be reclassified as a class belonging to the phylum Chloroflexota (formerly Chloroflexi). The bacteria Sphaerobacter thermophilus originally described as an Actinobacteria is now considered a Thermomicrobia.[4][7] In the same year, another strain of rose-pink thermophilic bacteria was isolated from Yellowstone National Park, which was named Thermobaculum terrenum.[8] Later analysis based on genome put this species under Thermomicrobia class.[9] However, the current standing of Thermobaculum terrenum is disputed.[10]

In 2012, a thermo-tolerant nitrite-oxidizing bacterium was isolated from a bioreactor, which was named Nitrolancetus hollandica and proposed as a novel species later in 2014.[11] While it has nitrite-oxidizing activity, which is unique in the Thermomicrobia class, it is placed under the Thermomicrobia class based on 16s rRNA phylogeny.[12]

In 2014, two thermophilic, Gram-positive, rod-shaped, non-spore-forming bacteria (strains KI3T and KI4T) isolated from geothermally heated biofilms growing on a tumulus in the Kilauea Iki pit crater on the flank of Kilauea Volcano (Hawai'i) were proposed as representatives of new species based on 16s rRNA phylogeny. The KI3T strain, later named as Thermomicrobium carboxidum, is closely related to Thermomicrobium roseum. The KI4T strain, later named as Thermorudis peleae, was proposed as a type strain of new genus Thermorudis.[13]

In 2015, a thermophilic bacteria strain WKT50.2 isolated from geothermal soil in Waitike (New Zealand) was proposed to be a novel species, later named Thermorudis pharmacophila. Phylogenic analysis based on 16s rRNA place it within Thermomicrobia class, as close relative to Thermorudis peleae.[5]

Characteristics

Living environment

Members of the class Thermomicrobia are broadly distributed across a wide range of both aquatic and terrestrial habitats. Thermomicrobium roseum was found in geothermally heated hot springs, Thermorudis pharmacophila and Thermobaculum terrenum from heated soils, and Thermomicrobium carboxidum and Thermorudis peleae from heated sediments[13][5][14] In addition, Sphaerobacter thermophilus was found in sewage sludge that went through thermophilic treatment.[15] The common features of their habitats include temperature ranging from around 65~75 °C and a pH around 6.0~8.0 (except for Nitrolancea hollandica which grow around 40 °C[11]).

Metabolism

Members of Thermomicrobia class have variation in their basic metabolism. Nitrolancetus hollandica has nitrifying activity that utilize NO2− as energy source, which is unique in the whole Chloroflexota phylum.[12] Thermomicrobium spp. and Sphaerobacter thermophilus have constitutive CO oxidizing not found in other species in this class.[13][16] However, species of this class do share some features, as listed below:

  • All members except Thermobaculum terrenum have inability to utilize some common monosaccharides (e.g. glucose, fructose, etc.) as sole carbon source.[6][12][13][5] The mechanisms behind this inability are currently unknown.

Antibiotic resistance

Members of Thermomicrobia class exhibit certain level of resistance against metronidazole and/or trimethoprim, which are clinically relevant for humans.[17][18] Thermomicrobium carboxidum and Thermorudis peleae show resistance against both of those antibiotics, while Sphaerobacter thermophilus shows resistance against only metronidazole.[5] Interestingly, Thermomicrobium roseum and Thermorudis pharmacophila have an increased growth in both metronidazole and trimethoprim, a rare trait even within antibiotic resistant bacteria.[5] The mechanisms behind are currently undocumented, and further study is required on this topic.

Cell envelope structure

Members of Thermomicrobia class have various Gram-staining results. Thermomicrobium roseum, Sphaerobacter thermophilus and Thermorudis pharmacophila are reported to be Gram-negative and have a typical layered diderm cell envelope structure.[3][4][5] However, their cell envelope composition are atypical compared to typical Gram-negative bacteria. Cell envelope of Thermomicrobium roseum lacks significant amount of peptidoglycan, which is fundamental for typical Gram-negative bacteria, while being rich in protein.[3] Membrane lipids of Thermomicrobium roseum are mostly long chain diols instead of glycerol-based lipids commonly found in bacteria.[19] The same feature was found in Sphaerobacter thermophilus and Thermorudis pharmacophila.[5] It was suggested that the high-protein and diol-based lipid composition are responsible for heat resistance of these bacteria.[4][20]

Meanwhile, other members of Thermomicrobia class are reported to be Gram-positive and have typical monoderm cell envelope.[8][12][13] There are some possible explanations of the inconsistency of Gram-staining result within the class. For Thermorudis pharmacophila, a possible explanation suggested by Houghton et al. is that it is actually an atypical monoderm bacterium, because its cell envelope contains amino acids usually associated with Gram-positive bacteria, have reaction to KOH, vancomycin and ampicillin, and lacks genes responsible for diderm formation.[5] It is also suggested that further study is required to resolve this problem, since the inconsistent reports of cell envelope structure are found for the whole Chloroflexota phylum.

Phylogeny


16S rRNA based LTP_08_2023[21][22][23] 120 marker proteins based GTDB 08-RS214 (28th April 2023).[24][25][26]
Thermomicrobia
Sphaerobacterales

Nitrolancea

Sphaerobacter

Thermomicrobiales

Thermalbibacter

Thermomicrobium

Thermorudis
Thermomicrobiales
Thermomicrobiaceae

Nitrolancea

Sphaerobacter

Thermomicrobium

Thermorudis

Taxonomy

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN)[27] and National Center for Biotechnology Information (NCBI).[28]

  • Order Sphaerobacterales Stackebrandt, Rainey & Ward-Rainey 1997
  • Order Thermomicrobiales Garrity & Holt 2002
    • Family Thermomicrobiaceae Garrity & Holt 2002
      • Genus Thermalbibacter Zhao et al. 2023
        • T. longus Zhao et al. 2023
      • Genus Thermomicrobium Jackson, Ramaley & Meinschein 1973[6]
        • T. carboxidum King & King 2014[13]
        • T. roseum Jackson, Ramaley & Meinschein 1973[6]
      • Genus Thermorudis King & King 2014[13]
        • T. peleae King & King 2014[13]
        • T. pharmacophila Houghton et al. 2015[5]

See also

Notes

  1. ↑ The above description does not take newly discovered species after 2004 into account.
  2. 1 2 Strain found at the National Center for Biotechnology Information (NCBI) but has no standing with the Bacteriological Code (1990 and subsequent Revision) as detailed by List of Prokaryotic names with Standing in Nomenclature (LPSN) as a result of the following reasons:

References

  1. ↑ Oren A, Garrity GM (2021). "Valid publication of the names of forty-two phyla of prokaryotes". Int J Syst Evol Microbiol. 71 (10): 5056. doi:10.1099/ijsem.0.005056. PMID 34694987.
  2. ↑ Garrity GM, Holt JG. (2001). "Class I. Thermomicrobia class. nov.". In Boone DR, Castenholz RW, Garrity GM. (eds.). Bergey's Manual of Systematic Bacteriology. Vol. 1 (The Archaea and the Deeply Branching and Phototrophic Bacteria) (2nd ed.). New York, NY: Springer. pp. 447–450.
  3. 1 2 3 4 Garrity GM, Holt JG (2001). "Phylum BVII. Thermomicrobia phy. nov.". In Boone DR, Castenholz RW, Garrity GM (eds.). Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria. New York: Springer.
  4. 1 2 3 4 Hugenholtz P, Stackebrandt E (November 2004). "Reclassification of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description)". International Journal of Systematic and Evolutionary Microbiology. 54 (Pt 6): 2049–51. doi:10.1099/ijs.0.03028-0. PMID 15545432.
  5. 1 2 3 4 5 6 7 8 9 10 Houghton KM, Morgan XC, Lagutin K, MacKenzie AD, Vyssotskii M, Mitchell KA, McDonald IR, Morgan HW, Power JF, Moreau JW, Hanssen E, Stott MB (December 2015). "Thermorudis pharmacophila sp. nov., a novel member of the class Thermomicrobia isolated from geothermal soil, and emended descriptions of Thermomicrobium roseum, Thermomicrobium carboxidum, Thermorudis peleae and Sphaerobacter thermophilus". International Journal of Systematic and Evolutionary Microbiology. 65 (12): 4479–87. doi:10.1099/ijsem.0.000598. hdl:10289/11806. PMID 26374291.
  6. 1 2 3 4 Jackson TJ, Ramaley RF, Meinschein WG (January 1973). "Thermomicrobium, a new genus of extremely thermophilic bacteria". International Journal of Systematic and Evolutionary Microbiology. 23 (1): 28–36. doi:10.1099/00207713-23-1-28.
  7. ↑ Boone DR, Baker CC (2002). "Validation of publication of new names and new combinations previously effectively published outside the IJSEM". International Journal of Systematic and Evolutionary Microbiology. 52 (Pt 3): 685–90. doi:10.1099/ijs.0.02358-0. PMID 12054225. Archived from the original on 6 June 2010.
  8. 1 2 Botero LM, Brown KB, Brumefield S, Burr M, Castenholz RW, Young M, McDermott TR (April 2004). "Thermobaculum terrenum gen. nov., sp. nov.: a non-phototrophic gram-positive thermophile representing an environmental clone group related to the Chloroflexi (green non-sulfur bacteria) and Thermomicrobia". Archives of Microbiology. 181 (4): 269–77. doi:10.1007/s00203-004-0647-7. PMID 14745485. S2CID 31431143.
  9. ↑ Kunisawa T (August 2011). "The phylogenetic placement of the non-phototrophic, Gram-positive thermophile 'Thermobaculum terrenum' and branching orders within the phylum 'Chloroflexi' inferred from gene order comparisons". International Journal of Systematic and Evolutionary Microbiology. 61 (Pt 8): 1944–53. doi:10.1099/ijs.0.026088-0. PMID 20833875.
  10. ↑ See the NCBI webpage on unclassified Terrabacteria group Data extracted from the "NCBI Taxonomy Browser". National Center for Biotechnology Information. Retrieved 2018-10-01.
  11. 1 2 Sorokin DY, Vejmelkova D, Lücker S, Streshinskaya GM, Rijpstra WI, Damste JS, Kleerbezem R, van Loosdrecht M, Muyzer G, Daims H (June 2014). "Nitrolancea hollandica gen. nov., sp. nov., a chemolithoautotrophic nitrite-oxidizing bacterium isolated from a bioreactor belonging to the phylum Chloroflexi". International Journal of Systematic and Evolutionary Microbiology. 64 (6): 1859–1865. doi:10.1099/ijs.0.062232-0. PMID 24573161.
  12. 1 2 3 4 5 6 Sorokin DY, Lücker S, Vejmelkova D, Kostrikina NA, Kleerebezem R, Rijpstra WI, Damsté JS, Le Paslier D, Muyzer G, Wagner M, van Loosdrecht MC, Daims H (December 2012). "Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi". The ISME Journal. 6 (12): 2245–56. doi:10.1038/ismej.2012.70. PMC 3504966. PMID 22763649.
  13. 1 2 3 4 5 6 7 8 King CE, King GM (August 2014). "Thermomicrobium carboxidum sp. nov., and Thermorudis peleae gen. nov., sp. nov., carbon monoxide-oxidizing bacteria isolated from geothermally heated biofilms". International Journal of Systematic and Evolutionary Microbiology. 64 (Pt 8): 2586–92. doi:10.1099/ijs.0.060327-0. PMID 24814334.
  14. ↑ Costa KC, Navarro JB, Shock EL, Zhang CL, Soukup D, Hedlund BP (May 2009). "Microbiology and geochemistry of great boiling and mud hot springs in the United States Great Basin". Extremophiles. 13 (3): 447–59. doi:10.1007/s00792-009-0230-x. PMID 19247786. S2CID 24375281.
  15. 1 2 3 Demharter W, Hensel R, Smida J, Stackebrandt E (May 1989). "Sphaerobacter thermophilus gen. nov., sp. nov. A deeply rooting member of the actinomycetes subdivision isolated from thermophilically treated sewage sludge". Systematic and Applied Microbiology. 11 (3): 261–6. doi:10.1016/S0723-2020(89)80023-2.
  16. ↑ Wu D, Raymond J, Wu M, Chatterji S, Ren Q, Graham JE, Bryant DA, Robb F, Colman A, Tallon LJ, Badger JH, Madupu R, Ward NL, Eisen JA (2009-01-16). "Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum". PLOS ONE. 4 (1): e4207. Bibcode:2009PLoSO...4.4207W. doi:10.1371/journal.pone.0004207. PMC 2615216. PMID 19148287.
  17. ↑ "Metronidazole Monograph for Professionals - Drugs.com". Drugs.com. Retrieved 2018-10-11.
  18. ↑ "Trimethoprim Monograph for Professionals - Drugs.com". Drugs.com. Retrieved 2018-10-11.
  19. ↑ Pond JL, Langworthy TA, Holzer G (March 1986). "Long-chain diols: a new class of membrane lipids from a thermophilic bacterium". Science. 231 (4742): 1134–6. Bibcode:1986Sci...231.1134P. doi:10.1126/science.231.4742.1134. JSTOR 1696788. PMID 17818542. S2CID 42023577.
  20. ↑ Pond JL, Langworthy TA (March 1987). "Effect of growth temperature on the long-chain diols and fatty acids of Thermomicrobium roseum". Journal of Bacteriology. 169 (3): 1328–30. doi:10.1128/jb.169.3.1328-1330.1987. PMC 211939. PMID 3818547.
  21. ↑ "The LTP". Retrieved 20 November 2023.
  22. ↑ "LTP_all tree in newick format". Retrieved 20 November 2023.
  23. ↑ "LTP_08_2023 Release Notes" (PDF). Retrieved 20 November 2023.
  24. ↑ "GTDB release 08-RS214". Genome Taxonomy Database. Retrieved 10 May 2023.
  25. ↑ "bac120_r214.sp_label". Genome Taxonomy Database. Retrieved 10 May 2023.
  26. ↑ "Taxon History". Genome Taxonomy Database. Retrieved 10 May 2023.
  27. ↑ J.P. Euzéby. "Thermomicrobia". List of Prokaryotic names with Standing in Nomenclature (LPSN). Retrieved 2022-07-20.
  28. ↑ Sayers; et al. "Thermomicrobia". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2022-03-20.
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