Asymmetrical utilization of chiral compounds has been sought on Mars as evidence for biological activity. This method was recently validated in glucose. Earth organisms utilize D-glucose, not L-glucose, a perfect asymmetry. In this study, we tested the method in lactate and found utilization of both enantiomers. Soil-, sediment-, and lake-borne microbial communities prefer D-lactate but can consume L-lactate if given extra time to acclimate. This situation is termed imperfect asymmetry. Future life-detection mission investigators need to be aware of imperfect asymmetry so as not to miss relatively subtle signs of life. Key Words: Chirality—Homochirality—Life detection—Atacama Desert. Astrobiology 10, 397–402.
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References
1.
BarkerS.B., SummersonW.H.1941. The colorimetric determination of lactic acid in biological material. J. Biol. Chem., 138:535–554.
2.
CompeauG., AlachiB.J., PlatsoukaE., LevyS.B.1988. Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl. Environ. Microbiol., 54:2432–2438.
3.
CristescuM.E.2008. D- and L-lactate dehydrogenases during invertebrate evolution. BMC Evol. Biol., 8. doi:10.1186/1471-2148-8-268.
DuncanS.H., LouisP., FlintH.J.2004. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl. Environ. Microbiol., 70:5810–5817.
6.
EvansJ.D., MartinS.A.1997. Factors affecting lactate and malate utilization by Selenomonas ruminantium. Appl. Environ. Microbiol., 63:4853–4858.
7.
FormisanoV., AtreyaS., EncrenazT., IgnatievN., GiurannaM.2004. Detection of methane in the atmosphere of Mars. Science, 306:1758–1761.
GlavinD.P., SchubertM., BottaO., KminekG., BadaJ.L.2001. Detecting pyrolysis products from bacteria on Mars. Earth Planet. Sci. Lett., 185:1–5.
10.
GoffinP.2004. Major role of NAD-dependent lactate dehydrogenases in aerobic lactate utilization in Lactobacillus plantarum during early stationary phase. J. Bacteriol., 186:6661–6666.
11.
GoffinP., DeghorainM., MainardiJ.L., TytgatI., Champomier-VergèsM.C., KleerebezemM., HolsP.2005. Lactate racemization as a rescue pathway for supplying D-lactate to the cell wall biosynthesis machinery in Lactobacillus plantarum. J. Bacteriol., 187:6750–6761.
12.
HalpernB., WestleyJ.W., AndersonP.J., LederbergJ.1966. Demonstration of the stereospecific action of microorganisms in soil by gas liquid chromatography. Anal. Biochem., 17:179–182.
13.
HinoT., KurodaS.1993. Presence of lactate dehydrogenase and lactate racemase in Megasphaera elsdenii grown on glucose or lactate. Appl. Environ. Microbiol., 59:255–259.
14.
HiyamaT., FukuiS., KitaharaK.1968. Purification and properties of lactate racemase from Lactobacillus sake. J. Biochem., 64:99–107.
15.
HoutkooperJ.M., Schulze-MakuchD.2007. A possible biogenic origin for hydrogen peroxide on Mars: the Viking results reinterpreted. Int. J. Astrobiology, 6:147–152.
16.
KelleyL.M., MeyerE.D., ZumbergeJ.E., BandurskiE.L., NagyB.1975. Stereoisomeric specificity and soil gas disequilibria: implications for martian life detection. Appl. Microbiol., 29:229–233.
17.
KleinH.P.1977. The Viking biological investigation: general aspects. J. Geophys. Res., 82:4677–4680.
18.
KleinH.P.1978. The Viking biological experiments on Mars. Icarus, 34:666–674.
19.
KochharS., HunzikerP.E., LeongmorgenthalerP., HottingerH.1992. Evolutionary relationship of NAD+-dependent D-lactate dehydrogenase—comparison of primary structure of 2-hydroxy acid dehydrogenases. Biochem. Biophys. Res. Commun., 184:60–66.
20.
Le BrasG., GarelJ.R.1991. Properties of D-lactate dehydrogenase from Lactobacillus bulgaricus: a possible different evolutionary origin for the D-lactate and L-lactate dehydrogenases. FEMS Microbiol. Lett., 79:89–93.
McKayC.P., GrunthanerF.J., LaneA.L., HerringM., BartmanR.K., KsendzovA., ManningC.M., LambJ.L., WilliamsR.M., RiccoA.J., ButlerM.A., MurrayB.C., QuinnR.C., ZentA.P., KleinH.P., LevinG.V.1998. The Mars Oxidant experiment (MOx) for Mars ’96. Planet. Space Sci., 46:769–777.
23.
MiltonR.C.D., MiltonS.C.F., KentS.B.H.1992. Total chemical synthesis of a D-enzyme—the enantiomers of HIV-1 protease show demonstration of reciprocal chiral substrate specificity. Science, 256:1445–1448.
24.
Navarro-GonzálezR., RaineyF.A., MolinaP., BagaleyD.R., HollenB.J., de la RosaJ., SmallA.M., QuinnR.C., GrunthanerF.J., CaceresL., Gomez-SilvaB., McKayC.P.2003. Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science, 302:1018–1021.
25.
OrenA., GurevichP.1995. Diversity of lactate metabolism in halophilic archaea. Can. J. Microbiol., 41:302–307.
26.
PassarellaS., de BariL., ValentiD., PizzutoR., PaventiG., AtlanteA.2008. Mitochondria and L-lactate metabolism. FEBS Lett., 582:3569–3576.
27.
StetterK.O., KandlerO.1973. Formation of D-lactic acid by lactobacilli and characterization of a lactic acid racemase from several streptobacteria. Arch. Microbiol., 94:221–247.
28.
SunH.J., SaccomannoV., HedlundB.P., McKayC.P.2009. Stereo-specific glucose consumption may be used to distinguish between chemical and biological reactivity on Mars: a preliminary test on Earth. Astrobiology, 9:443–446.
29.
TaguchiH., OhtaT.1991. D-Lactate dehydrogenase is a member of the D-isomer-specific 2-hydroxyacid dehydrogenase family—cloning, sequencing, and expression in Escherichia coli of the D-lactate dehydrogenase gene of Lactobacillus plantarum. J. Biol. Chem., 266:12588–12594.
30.
TraudtM., KleinbergI.1996. Stoichiometry of oxygen consumption and sugar, organic acid and amino acid utilization in salivary sediment and pure cultures of oral bacteria. Arch. Oral Biol., 41:965–978.
31.
WarmflashD., ChuH., SiebertJ., FoxG.E.2009. Life detection using glucose and tetrasaccharide enantiomer pairs. Astrobiology, 9:297–303.
32.
YangS.T., TangI.C.1991. Methanogenesis from lactate by a coculture of Clostridium formicoaceticum and Methanosarcina mazei. Appl. Microbiol. Biotechnol., 35:119–123.
