Aquificae

The Aquificae phylum is a diverse collection of bacteria that live in harsh environmental settings.[1][2] The name 'Aquificae' was given to this phylum based on an early genus identified within this group, Aquifex (“water maker”), which is able to produce water by oxidizing hydrogen.[3] They have been found in springs, pools, and oceans. They are autotrophs, and are the primary carbon fixers in their environments. These bacteria are Gram-negative, non-spore-forming rods.[4] They are true bacteria (domain Bacteria) as opposed to the other inhabitants of extreme environments, the Archaea.

Aquificae
Scientific classification
Domain:	Bacteria
Phylum:	Aquificae Reysenbach 2002 emend. Gupta & Lali 2014
Class:	Aquificae Reysenbach 2002 emend. Gupta & Lali 2014
Orders & Families
Aquificales Aquificaceae Hydrogenothermaceae Desulfurobacteriales Desulfurobacteriaceae Thermosulfidibacter
Synonyms
Aquificaeota Oren et al. 2015

Taxonomy

The Aquificae currently contain 15 genera and 42 validly published species.[5] The phylum comprises a single class and two orders.[6][7] Aquificales consists of the families Aquificaceae and Hydrogenothermaceae, while the Desulfurobacteriaceae are the only family within the Desulfobacteriales. Thermosulfidibacter takaii is not assigned to a family within the phylum based on its phylogenetic distinctness from both orders.[8] It is currently classified as a member of Aquificales, but it has shown more physiological similarity to the Desulfobacteriaceae.

Molecular signatures and phylogenetic position

Comparative genomic studies have identified several conserved signature indels (CSIs) that are specific for all species belonging to the phylum Aquificae and provide potential molecular markers.[7] The order Aquificales can be distinguished from Desulfobacteriales by several CSIs across different proteins that are specific for each group. Additional CSIs have been found at the family level, and can be used to demarcate Aquificae and Hydrogenothermaceae from all other bacteria.[7] In parallel with the observed CSI distribution, the orders within the Aquificae are also physiologically distinct from one another. Members of the Desulfurobacteriales are strict anaerobes that exclusively oxidize hydrogen for energy, whereas those belonging to the Aquificales are microaerophilic, and capable of oxidizing other compounds (such as sulfur or thiosulfate) in addition to hydrogen.[9][10][11]

Several CSIs have also been identified that are specific for the species from the Aquificae and provide potential molecular markers for this phylum.[1] Additionally, a 51-amino-acid insertion has been identified in SecA preprotein translocase which is shared by various members of the Aquificae, as well as two Thermotoga species. In the 16S rRNA gene trees, the Aquificae species branch in the proximity of the phylum Thermotogae (another phylum comprising hyperthermophilic organisms) close to the archaeal-bacterial branch point.[12][10] However, a close relationship of the Aquificae to the Thermotogae and the deep branching of the Aquificae is not supported by some phylogenetic studies based upon other gene/protein sequences[13][14][15][16] and also by CSIs in several highly conserved universal proteins.[17] Thus, the presence of the insertion in the Thermotoga species may be due to a horizontal gene transfer.[1] The deep branching of Aquificae species in the rRNA gene tree was ascribed to be an artefact resulting from the very high G+C content of their 16S-23S-5S operons.[17] In contrast to the very high G+C content of their rRNAs (i.e. more than 62%), which is required for stability of their secondary structures at high growth temperatures,[18] the inference that the Aquificae do not constitute a deep-branch lineage is also independently strongly supported by CSIs in a number of important proteins (viz. Hsp70, Hsp60, RpoB, RpoB and AlaRS), which support its placement in the proximity of the phylum Proteobacteria, particularly the Epsilonproteobacteria.[17] A specific relationship of the Aquificae to the Proteobacteria is supported by a two-amino-acid CSI in the protein inorganic pyrophosphatase, which is uniquely found in species from these two phyla.[17] Cavalier-Smith has also suggested that the Aquificae are closely related to the Proteobacteria.[19] In contrast to the above cited analyses that are based on a few indels or on single genes, analyses on informational genes, which appeared to be less often transferred to the Aquifex lineage than noninformational genes, most often placed the Aquificales close to the Thermotogales.[20] These authors explain the frequently observed grouping of Aquificae with Epsilonproteobacteria as result of frequent horizontal gene transfer due to shared ecological niches.

Along with the Thermotogae, the Aquificae are thermophilic eubacteria.[2]

Phylogeny

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN) [5] and National Center for Biotechnology Information (NCBI)[21] and the phylogeny is based on 16S rRNA-based LTP release 123 by The All-Species Living Tree Project [22] [23]

Thermosulfidibacter takaii     Desulfurobacteriaceae   Phorcysia thermohydrogeniphila       Desulfurobacterium thermolithotrophum         Desulfurobacterium atlanticum     Desulfurobacterium pacificum     Thermovibrio   T. ruber       Balnearium lithotrophicum       T. ammonificans     T. guaymasensis               Aquificales Hydrogenothermaceae   Persephonella hydrogeniphila       Persephonella marina       Persephonella guaymasensis       Venenivibrio stagnispumantis   Sulfurihydrogenibium   S. yellowstonense         S. kristjanssonii     S. subterraneum         S. azorense     S. rodmanii                 Aquificaceae   Hydrogenobaculum acidophilum     Hydrogenobacter   H. subterraneus       H. hydrogenophilus     H. thermophilus           Thermocrinis minervae       Thermocrinis ruber       Thermocrinis albus       Aquifex pyrophilus   Hydrogenivirga   H. calditorris     H. okinawensis

Note:
♠ Strain found at the National Center for Biotechnology Information (NCBI) but not listed in the List of Prokaryotic names with Standing in Nomenclature (LPSN)

Taxonomy

• Genus Thermosulfidibacter Nunoura et al. 2008
  • Species Thermosulfidibacter takaii Nunoura et al. 2008
• Order Desulfurobacteriales Gupta & Lali 2014
  • Family Desulfurobacteriaceae L'Haridon et al. 2006
    • Genus Balnearium Takai et al. 2003
      • Species Balnearium lithotrophicum Takai et al. 2003
    • Genus Desulfurobacterium L'Haridon et al. 1998 emend. L'Haridon et al. 2006
      • Species "D. crinifex" ♠ Alain et al. 2003
      • Species D. atlanticum L'Haridon et al. 2006
      • Species D. pacificum L'Haridon et al. 2006
      • Species D. thermolithotrophum L'Haridon et al. 1998 (type sp.)
    • Genus Phorcysia Pérez-Rodríguez et al. 2012
      • Species Phorcysia thermohydrogeniphila Pérez-Rodríguez et al. 2012
    • Genus Thermovibrio Huber et al. 2002
      • Species T. ammonificans Vetriani et al. 2004
      • Species T. guaymasensis L'Haridon et al. 2006
      • Species T. ruber Huber et al. 2002 (type sp.)
• Order Aquificales Reysenbach 2002 emend. Gupta & Lali 2014
  • Family Aquificaceae Reysenbach 2002
    • Genus Aquifex Huber and Stetter 1992
      • Species A. pyrophilus Huber and Stetter 1992 (type sp.)
      • Species "A. aeolicus" ♠ Huber and Stetter 2001
    • Genus Hydrogenivirga Nakagawa et al. 2004
      • Species H. calditorris Nakagawa et al. 2004 (type sp.)
      • Species H. okinawensis Nunoura et al. 2008
    • Genus Hydrogenobacter Kawasumi et al. 1984
      • Species H. hydrogenophilus (Kryukov et al. 1984) Stöhr et al. 2001
      • Species H. subterraneus Takai et al. 2001
      • Species H. thermophilus Kawasumi et al. 1984 (type sp.)
    • Genus Hydrogenobaculum Stöhr et al. 2001
      • Species Hydrogenobaculum acidophilum (Shima and Suzuki 1993) Stöhr et al. 2001
    • Genus Thermocrinis Huber et al. 1999
      • Species T. albus Eder and Huber 2002
      • Species T. jamiesonii Dodsworth et al. 2015
      • Species T. minervae Huber et al. 1999
      • Species T. ruber Huber et al. 1999 (type sp.)
  • Family Hydrogenothermaceae Eder and Huber 2003
    • Genus Hydrogenothermus Stöhr et al. 2001
      • Species Hydrogenothermus marinus Stöhr et al. 2001
    • Genus Persephonella Götz et al. 2002
      • Species P. hydrogeniphila Nakagawa et al. 2003
      • Species P. marina Götz et al. 2002 (type sp.)
      • Species P. guaymasensis Götz et al. 2002
    • Genus Sulfurihydrogenibium Takai et al. 2003 emend. O'Neill et al. 2008
      • Species S. azorense Aguiar et al. 2004 emend. Nakagawa et al. 2005
      • Species S. kristjanssonii Flores et al. 2008
      • Species S. rodmanii O'Neill et al. 2008
      • Species S. subterraneum Takai et al. 2003 emend. Nakagawa et al. 2005 (type sp.)
      • Species S. yellowstonense Nakagawa et al. 2005
    • Genus Venenivibrio Hetzer et al. 2008
      • Species Venenivibrio stagnispumantis Hetzer et al. 2008

References

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2. Horiike T, Miyata D, Hamada K, et al. (January 2009). "Phylogenetic construction of 17 bacterial phyla by new method and carefully selected orthologs". Gene. 429 (1–2): 59–64. doi:10.1016/j.gene.2008.10.006. PMC 2648810. PMID 19000750.
3. Huber R, Wilharm T, Huber D, Trincone A, Burggaf S, Konig H, Reinhard R, Rockinger I, Fricke H, Stetter K (1992). "Aquifex pyrophilus gen. nov. sp. nov., Represents a Novel Group of Marine Hyperthermophilic Hydrogen-Oxidizing Bacteria". Syst. Appl. Microbiol. 15 (3): 340–351. doi:10.1016/S0723-2020(11)80206-7.
4. L'Haridon, Reysenbach AL, Tindall BJ, Schönheit P, Banta A, Johnsen U, Schumann P, Gambacorta A, Stackebrandt E, Jeanthon C (December 2006). "Desulfurobacterium atlanticum sp. nov., Desulfurobacterium pacificum sp. nov. and Thermovibrio guaymasensis sp. nov., three thermophilic members of the Desulfurobacteriaceae fam. nov., a deep branching lineage within the bacteria". Int. J. Syst. Evol. Microbiol. 56 (Pt 12): 2843–2852. doi:10.1099/ijs.0.63994-0. PMID 17158986.
5. J.P. Euzéby. "Aquificae". List of Prokaryotic names with Standing in Nomenclature (LPSN). Archived from the original on 2011-06-13. Retrieved 2016-09-09.
6. Oren A, Garrity GM (2015). "List of new names and new combinations previously effectively, but not validly, published". Int. J. Syst. Evol. Microbiol. 65 (7): 2017–2025. doi:10.1099/ijs.0.000317. PMC 5817221. PMID 28891789.
7. Gupta RS, Lali R (September 2013). "Molecular signatures for the phylum Aquificae and its different clades: proposal for division of the phylum Aquificae into the emended order Aquificales, containing the families Aquificaceae and Hydrogenothermaceae, and a new order Desulfurobacteriales ord. nov., containing the family Desulfurobacteriaceae". Antonie van Leeuwenhoek. 104 (3): 349–368. doi:10.1007/s10482-013-9957-6. PMID 23812969.
8. Nunoura T, Oida H, Miyazaki M, Suzuki Y (March 2008). "Thermosulfidibacter takaii gen. nov., sp. nov., a thermophilic, hydrogen-oxidizing, sulfur-reducing chemolithoautotroph isolated from a deep-sea hydrothermal field in the Southern Okinawa Trough". Int. J. Syst. Evol. Microbiol. 58 (Pt 3): 659–665. doi:10.1099/ijs.0.65349-0. PMID 18319474.
9. Guiral M, Prunetti L, Aussignargues C, Ciaccafava A, Infossi P, Ilbert M, Lojou E, Giudici-Orticoni MT (2012). The hyperthermophilic bacterium Aquifex aeolicus: from respiratory pathways to extremely resistant enzymes and biotechnological applications. Adv. Microb. Physiol. Advances in Microbial Physiology. 61. pp. 125–194. doi:10.1016/B978-0-12-394423-8.00004-4. ISBN 9780123944238. PMID 23046953.
10. Reysenbach, A.-L. (2001) Phylum BII. Thermotogae phy. nov. In: Bergey's Manual of Systematic Bacteriology, pp. 369-387. Eds D. R. Boone, R. W. Castenholz. Springer-Verlag: Berlin.
11. Gupta, RS (2014) The Phylum Aquificae. The Prokaryotes 417-445. Springer Berlin Heidelberg.
12. Huber, R. and Hannig, M. (2006) Thermotogales. Prokaryotes 7: 899-922.
13. Klenk, H. P., Meier, T. D., Durovic, P. and others (1999) RNA polymerase of Aquifex pyrophilus: Implications for the evolution of the bacterial rpoBC operon and extremely thermophilic bacteria. J Mol Evol 48: 528-541.
14. Gupta, R. S. (2000) The phylogeny of Proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24: 367-402.
15. Ciccarelli, F. D., Doerks, T., von Mering, C., Creevey, C. J., Snel, B., and Bork, P. (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311: 1283-1287.
16. Di Giulio, M. (2003) The universal ancestor was a thermophile or a hyperthermophile: Tests and further evidence. J Theor Biol 221: 425-436.
17. Griffiths, E. and Gupta, R. S. (2004) Signature sequences in diverse proteins provide evidence for the late divergence of the order Aquificales. International Microbiol 7: 41-52.
18. Meyer, T. E. and Bansal, A. K. (2005) Stabilization against hyperthermal denaturation through increased CG content can explain the discrepancy between whole genome and 16S rRNA analyses. Biochemistry 44: 11458-11465.
19. Catalogue of Organisms: Standing the Heat
20. Boussau B, Guéguen L, Gouy M. Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of Aquificales in the phylogeny of Bacteria. BMC Evol Biol. 2008 Oct 3;8:272. doi:10.1186/1471-2148-8-272.
21. Sayers; et al. "Aquificae". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2016-09-09.
22. All-Species Living Tree Project."16S rRNA-based LTP release 123 (full tree)" (PDF). Silva Comprehensive Ribosomal RNA Database. Retrieved 2016-09-09.
23. Ludwig, W.; Euzéby, J. & Whitman W.B. (2008). "Bergey's Taxonomic Outlines: Volume 4 - Draft Taxonomic Outline of the Bacteroidetes, Planctomycetes, Chlamydiae, Spirochaetes, Fibrobacteres, Fusobacteria, Acidobacteria, Verrucomicrobia, Dictyoglomi, and Gemmatimonadetes" (PDF). Bergey's Manual Trust: 15. Archived from the original (PDF) on 2009-04-24. Retrieved 2011-06-27.