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.

Stereospecificity control in aminoacyl-tRNA-synthetases: new evidence of d-amino acids activation and editing

“…Recent data show that a prevalence of one amino acid enantiomer may lead to toxicity for a different one (15). Intensive studies of d -amino acids’ role discovered an effective enzymatic racemization mechanism in the archaeon, Methanococcus maripaludis (16) and in a yeast, Schizosaccharomyces pombe (17), leading to a conversion of d -alanine ( d -Ala) to l -alanine ( l -Ala), which is an unusual use of the d -enantiomer as a nitrogen source.…”

The UK Centre for Astrobiology: A Virtual Astrobiology Centre. Accomplishments and Lessons Learned, 2011–2016

“…Work has investigated the habitability of pH-neutral environments prevalent during the Noachian on Mars and the plausible redox couples for life, including the iron cycle (Nixon et al, 2012 ). UKCA has sought to understand what factors might limit microbial metabolisms on Mars, such as the presence of microbial toxins (Nixon et al, 2013 ; Nixon and Cockell, 2015 ). UKCA has been involved in using data from Mars missions, such as the NASA Mars Science Laboratory (Curiosity rover), to understand the habitability of present-day Mars (Martin-Torres et al, 2015 ).…”

Low potency toxins reveal dense interaction networks in metabolism

“…Such a hypothesis has not been tested experimentally as far as I know, except in so far as low affinity binding of small molecules to proteins is commonly observed as noted above, although it has been observed that D-amino acids are mildly toxic to a wide range of microorganisms compared to their L-enantiomers [ 73 ]. In principle the low millimolar binding of small ligands to proteins could be tested computationally using molecular docking software, by trying to dock molecules known to not be ligands for a protein to that protein.…”