title: Nonproteinogenic D-amino acids at millimolar concentrations are a toxin for anaerobic microorganisms relevant to early Earth and other anoxic planets.
abstract: The delivery of extraterrestrial organics to early Earth provided a potentially important source of carbon and energy for microbial life. Optically active organic compounds of extraterrestrial origin exist in racemic form, yet life on Earth has almost exclusively selected for L- over D-enantiomers of amino acids. Although D-enantiomers of proteinogenic amino acids are known to inhibit aerobic microorganisms, the role of concentrated nonproteinogenic meteoritic D-amino acids on anaerobic metabolisms relevant to early Earth and other anoxic planets such as Mars is unknown. Here, we test the inhibitory effect of D-enantiomers of two nonproteinogenic amino acids common to carbonaceous chondrites, norvaline and α-aminobutyric acid, on microbial iron reduction. Three pure strains (Geobacter bemidjiensis, Geobacter metallireducens, Geopsychrobacter electrodiphilus) and an iron-reducing enrichment culture were grown in the presence of 10 mM D-enantiomers of both amino acids. Further tests were conducted to assess the inhibitory effect of these D-amino acids at 1 and 0.1 mM. The presence of 10 mM D-norvaline and D-α-aminobutyric acid inhibited microbial iron reduction by all pure strains and the enrichment. G. bemidjiensis was not inhibited by either amino acid at 0.1 mM, but D-α-aminobutyric acid still inhibited at 1 mM. Calculations using published meteorite accumulation rates to the martian surface indicate D-α-aminobutyric acid may have reached inhibitory concentrations in little over 1000 years during peak infall. These data show that, on a young anoxic planet, the use of one enantiomer over another may render the nonbiological enantiomer an environmental toxin. Processes that generate racemic amino acids in the environment, such as meteoritic infall or impact synthesis, would have been toxic processes and could have been a selection pressure for the evolution of early racemases.
authors.affiliation: UK Centre for Astrobiology, School of Physics and Astronomy, University of Edinburgh , Edinburgh, UK .
authors.forename: Sophie L
authors.initials: SL
authors.lastname: Nixon
authors.forename: Charles S
authors.initials: CS
authors.lastname: Cockell
mesh_terms: D000613:Aminobutyrates / Q000737:chemistry / Q000633:toxicity*; D000693:Anaerobiosis; D001272:Atmosphere; D001421:Bacteria, Anaerobic / Q000145:classification / Q000187:drug effects* / Q000378:metabolism; D004305:Dose-Response Relationship, Drug; D018534:Earth, Planet; D007501:Iron / Q000378:metabolism; D010084:Oxidation-Reduction; D010802:Phylogeny; D013237:Stereoisomerism; D014633:Valine / Q000031:analogs & derivatives* / Q000737:chemistry / Q000633:toxicity
chemical_list: D000613:Aminobutyrates; C012223:alpha-aminobutyric acid; C005313:norvaline; D007501:Iron; D014633:Valine