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1 Department of Environmental Science, Policy and Management, 151 Hilgard Hall, University of California Berkeley, Berkeley, CA 94720-3110, USA
2 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
Correspondence
Philip Hugenholtz
phugenholtz{at}lbl.gov
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Present address: DOE Joint Genome Institute, 2800 Mitchell Creek Bldg 400-404, Walnut Creek, CA 94598, USA. 
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Sphaerobacter thermophilus DSM 20745T is AJ420142.
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). Comparative analysis of a partial 16S rRNA sequence obtained by reverse transcriptase sequencing (GenBank/EMBL/DDBJ accession no. X53210) suggested, at the time, that S. thermophilus was the most deeply branching member of the phylum Actinobacteria (high-G+C, Gram-positive bacteria; Demharter et al., 1989). This phylum-level assignment has been disseminated through the literature (Carreto et al., 1996; Embley & Stackebrandt, 1994; Monciardini et al., 2003; Rainey & Stackebrandt, 1993; Rappé et al., 1999; Shooner & Tyagi, 1995; Wiegel, 1998), culminating in a formal classification as a novel suborder of the Actinobacteria (Stackebrandt et al., 1997). However, the initial analysis by Demharter et al. (1989) was compromised by insufficient reference sequences (outgroups) and, as more 16S rRNA gene sequences have become available, it is apparent that S. thermophilus is not reproducibly affiliated with the Actinobacteria and is instead a member of the phylum Chloroflexi (green non-sulfur bacteria; Björnsson et al., 2002; Hugenholtz et al., 1998).
We have obtained an almost complete 16S rRNA gene sequence for the type strain of S. thermophilus (DSM 20745T) using methods described previously (Rainey et al., 1996) and confirm that its phylogenetic placement is within the Chloroflexi (Fig. 1), on the basis of evolutionary distance and Bayesian inference as previously described (Janssen & Hugenholtz, 2003). Fig. 1 shows only the Chloroflexi phylum sequences (ingroup) used in the analysis; they were rigorously tested for monophyly using a variety of bacterial outgroup sequences representing multiple phyla (not shown; datasets available on request), as described previously (Dalevi et al., 2001).
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), which it resembles phenotypically. Both are thermophilic, obligately aerobic, chemoheterotrophic, catalase-positive, non-motile, non-spore-forming, short irregular-shaped rods with similar DNA G+C content (Demharter et al., 1989; Garrity & Holt, 2001b). The cell membrane of T. roseum contains distinctive long-chain diols instead of the familiar glycerol-based lipids (Pond et al., 1986) and these have been postulated to contribute to membrane stabilization at high temperatures (Pond & Langworthy, 1987). S. thermophilus has not been investigated for its cell membrane composition, but given its relationship to T. roseum and the fact that it is a thermophile, it may also contain diol-based lipids.
T. roseum has long been recognized to be affiliated with the phylum Chloroflexi on the basis of 16S rRNA comparative analysis (Woese, 1987), but is currently classified in its own bacterial phylum, Thermomicrobia (Garrity & Holt, 2001b). We propose to transfer the class Thermomicrobia to the phylum Chloroflexi to acknowledge this phylogenetic relationship formally (Fig. 1). In addition to the class Thermomicrobia, at least four other major lineages exist in the phylum Chloroflexi (Fig. 1), three of which now have cultivated representatives: the well-characterized class Chloroflexi, containing the phototrophic genera Chloroflexus, Chloronema, Heliothrix and Oscillochloris and the chemoheterotrophic genus Herpetosiphon (Garrity & Holt, 2001a); the ‘Dehalococcoidetes’, containing the tetrachloroethene-respiring coccus ‘Dehalococcoides ethenogenes’ (Maymó-Gatell et al., 1997); and, most recently, the ‘Anaerolineae’, containing the thermophilic filamentous bacteria Anaerolinea thermophila and Caldilinea aerophila (Sekiguchi et al., 2003). The ‘Anaerolineae’ are not monophyletic in all analyses (note node support <90 % in Fig. 1) and may need to be subdivided as new sequences come to hand. Detailed comparative studies of S. thermophilus and other members of the Chloroflexi may reveal unifying chemotaxonomic and ultrastructural features of this interesting phylum. For example, some members of the Chloroflexi, including S. thermophilus, have unusual cell envelopes rich in protein and lacking significant amounts of peptidoglycan (Demharter et al., 1989; Maymó-Gatell et al., 1997; Merkel et al., 1980).
We conclude, on the basis of 16S rRNA gene sequence comparative analysis, that S. thermophilus should be reassigned to the class Thermomicrobia in the phylum Chloroflexi. We suggest retaining the order and family proposed for S. thermophilus (Sphaerobacterales and Sphaerobacteraceae, respectively; Stackebrandt et al., 1997) in the class Thermomicrobia until a more rigorous comparison of S. thermophilus and T. roseum is performed and further representatives of this class are characterized.
Emended description of the phylum Chloroflexi Garrity and Holt 2001
The phylum Chloroflexi is a deep-branching lineage of the Bacteria. On the basis of comparative 16S rRNA gene sequence analysis of isolates and environmental clones, the phylum can be divided into at least five major subdivisions, including the classes Chloroflexi and Thermomicrobia. Mostly Gram-negative, filamentous bacteria with unusual cell envelopes. No peptidoglycan or atypical peptidoglycan present in cell walls. Lipopolysaccharide-containing outer membrane not present in studied representatives.
Emended description of the class Thermomicrobia Garrity and Holt 2001
The class Thermomicrobia subdivides into two orders with validly published names: Thermomicrobiales Garrity and Holt 2001 and Sphaerobacterales Stackebrandt, Rainey and Ward-Rainey 1997. Pleomorphic, non-motile, non-spore-forming rods. Atypical proteinaceous cell walls.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Carreto, L., Moore, E., Nobre, M. F., Wait, R., Riley, P. W., Sharp, R. J. & da Costa, M. S. (1996). Rubrobacter xylanophilus sp. nov., a new thermophilic species isolated from a thermally polluted effluent. Int J Syst Bacteriol 46, 460–465.
Dalevi, D., Hugenholtz, P. & Blackall, L. L. (2001). A multiple-outgroup approach to resolving division-level phylogenetic relationships using 16S rDNA data. Int J Syst Evol Microbiol 51, 385–391.[Abstract]
Demharter, W., Hensel, R., Smida, J. & Stackebrandt, E. (1989). Sphaerobacter thermophilus gen. nov., sp. nov., a deeply rooting member of the Actinomycetes subdivision isolated from thermophilically treated sewage sludge. Syst Appl Microbiol 11, 261–266.
Embley, T. M. & Stackebrandt, E. (1994). The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48, 257–289.[Medline]
Garrity, G. M. & Holt, J. G. (2001a). Phylum BVI. Chloroflexi phy. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, p. 427. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
Garrity, G. M. & Holt, J. G. (2001b). Phylum BVII. Thermomicrobia phy. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, p. 447. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
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Pond, J. L. & Langworthy, T. A. (1987). Effect of growth temperature on the long-chain diols and fatty acids of Thermomicrobium roseum. J Bacteriol 169, 1328–1330.
Pond, J. L., Langworthy, T. A. & Holzer, G. (1986). Long-chain diols: a new class of membrane lipids from a thermophilic bacterium. Science 231, 1134–1136.
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Rappé, M. S., Gordon, D. A., Vergin, K. L. & Giovannoni, S. J. (1999). Phylogeny of actinobacteria small subunit (SSU) rRNA gene clones recovered from marine bacterioplankton. Syst Appl Microbiol 22, 106–112.
Sekiguchi, Y., Yamada, T., Hanada, S., Ohashi, A., Harada, H. & Kamagata, Y. (2003). 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. Int J Syst Evol Microbiol 53, 1843–1851.
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