Comment on Tocheva Et Al. “Sporulation, Bacterial Cell

CORRESPONDENCE LINK TO ORIGINAL ARTICLE

of mycobacterial Rv0899 with proteobacterial outer-membrane protein A (OmpA) proteins Comment on Tocheva et al. (highlighted by Tocheva et al.1), seems to reflect its function as a periplasmic peptidoglycan- “Sporulation, bacterial cell envelopes binding domain, but its overall topology and location remain unclear9. and the origin of life” Cumulatively, these observations argue against a common evolutionary history for the MOM of Corynebacterineae and the outer Iain C. Sutcliffe and Lynn G. Dover membranes in other diderm bacteria. Thus, we argue, in contrast to the conclusions of In their recent Opinion article (Sporulation, the suborder Corynebacterineae challenges Tocheva et al.1, that structurally distinct outer bacterial cell envelopes and the origin of life. these assumptions. The ‘mycolata’ are sig- membranes probably evolved at least twice. Nat. Rev. Microbiol. 14, 535–542 (2016))1, nificant because they belong to the predomi- Iain C. Sutcliffe and Lynn G. Dover are at the Faculty of Tocheva and colleagues build on their elegant nantly monoderm phylum Actinobacteria and Health and Life Sciences, Northumbria University, electron cryotomography studies to derive contain several major pathogens, including Newcastle Upon Tyne NE1 8ST, UK. an intriguing hypothesis that sporulation in Mycobacterium tuberculosis. Several lines of Correspondence to I.C.S. a primordial monoderm bacterium (having evidence support the uniqueness of the MOM. [email protected] a single membrane) could have resulted in First, mycolic acids are structurally distinct, doi:10.1038/nrmicro2016.113 the evolution of sporulating diderm bacte- being formed from condensed fatty acids4. Published online 25 Jul 2016 ria (having a double membrane) and thus Second, in contrast to the outer membranes 1. Tocheva, E. I., Ortega, D. R. & Jensen, G. J. all extant bacteria. The evolution of outer of all other diderm bacteria, mycolic acids Sporulation, bacterial cell envelopes and the origin of life. Nat. Rev. Microbiol. 14, 535–542 (2016). membranes as a consequence of the topog- are the only outer-membrane lipids that are 2. Albertsen, M. et al. Genome sequences of rare, raphy of sporulation is a plausible hypoth- described as being covalently anchored to the uncultured bacteria obtained by differential coverage 4,5 binning of multiple metagenomes. Nat. Biotechnol. esis; however, it should be highlighted that underlying arabinogalactan–peptidoglycan , 31, 533–538 (2013). Tocheva et al. consider a relatively limited which results in a unique architecture that 3. Hug, L. A. et al. A new view of the tree of life Nat. Microbiol. 1, 16048 (2016). range of the known and candidate phyla in is unlikely to have arisen from remodelling 4. Dover, L. G., Cerdeno-Tarraga, A. M., Pallen, M. J., their model. Thus, it will be of interest to see of typical outer membranes, as suggested by Parkhill, J. & Besra, G. S. Comparative cell wall core 1 biosynthesis in the mycolated pathogens, how their hypothesis stands up when tested Tocheva et al. Third, all other characterized Mycobacterium tuberculosis and Corynebacterium against expanded phylogenetic analyses; for outer membranes contain BamA family pro- diphtheriae. FEMS Microbiol. Rev. 28, 225–250 (2004). example, including the many new phyla that teins, which have a central role in β-barrel 5. Sutcliffe, I. C. A phylum level perspective on bacterial were identified in recent large-scale genomic protein insertion, along with several special- cell envelope architecture. Trends Microbiol. 18, 5,6 464–470 (2010). analyses, which include novel monoderm ized protein secretion systems . It is notable 6. Sutcliffe, I. C. Cell envelope architecture in the phyla and possibly phyla with novel cell that neither BamA proteins nor type I–VI Chloroflexi: a shifting frontline in a phylogenetic turf 2,3 war. Environ. Microbiol. 13, 279–282 (2011). envelope architectures . secretion systems have been identified in any 7. Abby, S. S. et al. Identification of protein secretion Although the hypothesis of Tocheva et al.1 mycolata5–7. Although bioinformatic evidence systems in bacterial genomes. Sci. Rep. 6, 23080 (2016). 8. Niederweis, M., Danilchanka, O., Huff, J., may help to explain the evolution of most types suggests that proteins with high β-sheet con- Hoffmann, C. & Engelhardt, H. Mycobacterial outer of outer membrane, we question their sugges- tent are found in the MOM, relatively few membranes: in search of proteins. Trends Microbiol. 18, 109–116 (2010). tions that all diderm bacteria have arisen from MOM proteins have been characterized in 9. Yao, Y., Barghava, N., Kim, J., Niederweis, M. an ancestral sporulating diderm and that outer detail, and orthology with β-barrels in other & Marassi, F. M. Molecular structure and peptidoglycan recognition of Mycobacterium membranes have probably only evolved once. membranes cannot be assumed. Notably, the tuberculosis ArfA (Rv0899). J. Mol. Biol. 416, As briefly acknowledged by Tocheva et al., structures of MOM porins differ from the 208–220 (2012). the uniqueness of the mycolic acid-based canonical β-barrels of porins in other diderm Competing interests statement outer membranes (MOMs) of members of taxa8. The homology of the carboxyl terminus The authors declare no competing interests.