Andreas Natsch and Roger Emter. Philosophical Transactions of the Royal Society B: Biological Sciences, April 20 2020. https://doi.org/10.1098/rstb.2019.0269
Abstract: Human body odour is dominated by the scent of specific odourants emanating from specialized glands in the axillary region. These specific odourants are produced by an intricate interplay between biochemical pathways in the host and odour-releasing enzymes present in commensal microorganisms of the axillary microbiome. Key biochemical steps for the release of highly odouriferous carboxylic acids and sulfur compounds have been elucidated over the past 15 years. Based on the profound molecular understanding and specific analytical methods developed, evolutionary questions could be asked for the first time with small population studies: (i) a genetic basis for body odour could be shown with a twin study, (ii) no effect of genes in the human leukocyte antigen complex on the pattern of odourant carboxylic acid was found, and (iii) loss of odour precursor secretion by a mutation in the ABCC11 gene could explain why a large fraction of the population in the Far East lack body odour formation. This review summarizes what is currently known at the molecular level on the biochemistry of the formation of key odourants in the human axilla. At the same time, we present for the first time the crystal structure of the Nα-acyl-aminoacylase, a key human odour-releasing enzyme, thus describing at the molecular level how bacteria on the skin surface have adapted their enzyme to the specific substrates secreted by the human host.
12. In the light of evolution—axilla odour as an evolutionary puzzle
In this review, we tried to give a comprehensive review on what is known of the biochemistry of human axilla odour formation and detection. We have already alluded to the potential evolutionary implications of these findings in the different sections above and will now summarize the key findings in the evolutionary context.
We highlighted the different specific odourants that are released as specific precursors by specialized glands. Combined with the fact that these precursors seem to be produced locally, axillary glands indeed appear to be a specialized metabolic organ producing these compounds for local secretion.
Multiple enzymes and transport proteins of the host are involved in scent release—some of these have already been characterized biochemically with in vitro experiments (ABCC11 and GGT1), while others can only be inferred based on what is known on the biosynthesis of related conjugates investigated especially in the toxicological field.
On the receiver side, the high sensitivity of the human nose (and hence the corresponding olfactory receptors) for axillary odourants also indicates a specific adaptation of our olfactory receptor repertoire to these human odourants, although further work is required on this aspect truly to explain the high sensitivity at the receptor level.
Taken together, the above observations on a specific and complex biochemistry for odour formation and detection in the human body suggest that axilla odours must have had an adaptive function in human evolutionary history. We contrasted this observation to other general ‘malodours’ such as foot, faecal or breath odours that can largely be explained by common bacterial catabolism of excess proteins, and no specific evolutionary adaptation is required to lead to such odours as simple by-products of the catabolism of residual proteins by opportunistic bacteria. The fact that our sense of smell is particularly tuned to those odours, too, as warning signals of decay also has evolutionary implications, but that's another story.
Turning from the human host to the commensal bacteria, an interesting case for coevolution could be described. The bacteria have highly specialized enzymes and transport proteins for precursor uptake and odour release. The analysis of the spectrum of odourant precursors released and the substrate specificity of the bacterial enzyme N-AGA reveals a close match of the substrate spectrum offered by the host and the substrate specificity of the bacterial enzyme. This could be further corroborated by the data on the crystal structure of the enzyme described herein for the first time: the Gln residue conserved in all acid precursors is tightly bound by an intricate network of hydrogen bonds in the active site explaining the high substrate specificity for Gln conjugates, while there is ample space for the binding of different hydrophobic residues found in the different substrates offered in this ecological niche by the human host.
We had found that the individual-specific odourtype is stable and genetically determined. This indicates that axilla odours can reveal individual-specific information and could, in principle, contribute to kin recognition. To what extent body odours were indeed a contributing factor in social communication in prehistoric societies may be difficult to assess, yet the stable, genetically determined pattern at least indicates that body odours could have had such a function based on the underlying (bio)chemistry.
While the observations summarized above all support the case for an adaptive function of axillary odours in an evolutionary context, the ABCC11 mutation, which confers an almost odourless phenotype and that has rapidly spread in human populations in the Far East, is telling an opposing story. The rapid spread of the haplotype containing this mutation points to a strong selection pressure and may indicate that axilla odours had already become an unwanted trait in early agrarian societies living in closer proximity. The reduced sensory capacity to smell the conspecific as revealed by high anosmia rates for body odours points in a similar direction: a loss of importance of chemical communication through axilla odours in recent evolutionary history, which now is also reflected in a widespread use of deodourants in contemporary societies. In Japan, where the frequency of the mutated ABCC11 haplotype is high, but has not reached 100%, individuals with a functional ABCC11 allele frequently undergo surgery [63,64] to remove axillary glands. Surgery is even covered by social security as axilla odours owing to a functional ABCC11 allele are perceived as a disease. Thus, axillary odours appear as a fascinating trace of our evolutionary past having largely lost their role in the contemporary context.
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