ReviewPeptidoglycan in eukaryotes: Unanswered questions
Graphical abstract
Introduction
Most bacteria have a peptidoglycan as an important constituent of the cell wall. It can be regarded as forming a giant molecule enclosing the cell. Even bacteria of the phylum Chlamydiae, which were thought to lack it, have recently been found to have peptidoglycan in their cell walls. This peptidoglycan contains D-alanyl-D-alanine groups, many of them only temporarily, until the terminal D-alanine is split off during crosslinking to an adjacent peptide chain. Incidentally, penicillin owes its antibiotic property to its similarity to this D-alanyl-D-alanine motif, which causes it to block the final step of peptidoglycan synthesis (Tipper and Strominger, 1965; Fishovitz et al., 2015, Fig. 1). Bacterial peptidoglycan also contains a D-glutamyl group, and in some cases, residues of D-aspartic acid, D-serine, D-glutamic acid or D-ornithine. The peptidoglycan of the cyanobacterium Synechocystis sp. strain PCC 6714 contains slightly more D-glutamic acid than D-alanine (Jürgens et al., 1983). For a detailed account of peptidoglycans in various bacteria, see Vollmer (2015).
Much research has been done, especially for medical reasons, on bacterial peptidoglycan. One question that has never to my knowledge been confronted is: Why does it contain D-amino acids? This may appear to be an unnecessary complication, since D-amino acids are usually more complicated to produce than L-amino acids. They are either synthesized from L-amino acids by racemases, or from 2-keto acids by D-amino acid transferases or D-amino acid dehydrogenases. Does it have to do with the chirality (handedness) of the carbohydrate part of peptidoglycan? Despite many reports and detailed reviews on peptidoglycan structure, e.g., Lovering et al. (2012), this question has not been fully resolved.
Section snippets
Peptidoglycan in some eukaryotic algae, not in others
Chloroplasts are derived from cyanobacteria, which also have peptidoglycan in their cell walls. Peptidoglycan is lacking in the green algal division Chlorophyta (Grosche and Rensing, 2017), but has been retained in the chloroplasts of the other green algae in the division Streptophyta (Takano and Takechi, 2010; Takano et al., 2018). It is also retained in Glaucophyta (Higuchi et al., 2016), but not in Rhodophyta (Grosche and Rensing, 2017).
Rhodophyta are mostly marine species (although
Peptidoglycan in lower land plants
The peptidoglycan has also been found in lower land plants (of which the extant representatives, apart from algae, are the bryophytes) that have evolved from the streptophyte algae (Hirano et al., 2016, Sato and Takano, 2017). All the way through evolution to mosses, the D-alanyl-D-alanine motif has been retained (Hirano et al., 2016), see Fig. 2.
Peptidoglycan in lycophytes
From the most primitive land plants, evolution has followed two main tracks: the lycophyte line and the pteridophyte-seed plant line. Peptidoglycan has not been observed directly in lycophytes, but its presence can be inferred from the toxicity of D-cycloserine and ampicillin (Izumi et al. 2003; 2008). D-cycloserine is an inhibitor of D-alanine-D-alanyl ligase involved in peptidoglycan synthesis. However, it also inhibits alanine racemase (e.g., Azam and Jayaram, 2016), and has a number of
Genes for peptidoglycan synthesis in seed plants
Can we be sure that peptidoglycan is not retained on the evolutionary track leading to seed plants, or has it, for some reason escaped detection? According to Lin et al. (2017) all of the genes necessary for peptidoglycan synthesis are present in the conifers Picea abies and Pinus taeda; however, it cannot be ruled out that some of them are pseudogenes, which would prevent peptidoglycan synthesis. It could be worth looking chemically, by electron microscopy, and by antibiotic tests, for
Conclusion
In conclusion, the presence of peptidoglycan in eukaryotes raises several questions that have not yet been answered. A major remaining question is: Why has peptidoglycan been retained along some lineages over hundreds of millions of years of evolution, but been quickly eliminated in other lineages?
Conflicts of interest
None.
Acknowledgement
I thank Dr Richard L. McKenzie for improving my English.
Lars Olof Björn was born in 1936 on the island of Gotland in the middle of the Baltic. After studies in Lund (Sweden), Berkeley, and at the Carnegie Institution of Washington (Dept. of Plant Science at Stanford), including a Ph.D. from Lund, he was professor 1971–1972 of plant physiology in Copenhagen, 1972–2001 of botany in Lund, and 2006–2010 of plant physiology in Guangzhou (China). He is now active as emeritus at Lund University. He has authored and coauthored a number of books, primarily
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Lars Olof Björn was born in 1936 on the island of Gotland in the middle of the Baltic. After studies in Lund (Sweden), Berkeley, and at the Carnegie Institution of Washington (Dept. of Plant Science at Stanford), including a Ph.D. from Lund, he was professor 1971–1972 of plant physiology in Copenhagen, 1972–2001 of botany in Lund, and 2006–2010 of plant physiology in Guangzhou (China). He is now active as emeritus at Lund University. He has authored and coauthored a number of books, primarily about light and life, most recently together with Dmitry Shevela and Govindjee “Photosynthesis: Energy for the biosphere and mankind” (2019). He has been a member of the Royal Swedish Academy of Science since 1982.