Direct and indirect formation of organohalogens by microorganisms
Final Report Abstract
Salt lake sediments in Western Australia are a natural source of volatile halogenated hydrocarbons to the atmosphere. Our experiments demonstrated that biotic mechanisms are predominant and that abiotic mechanisms contribute only to a minor extent to the overall formation in the Western Australian salt lake sediments. The addition of lactate/acetate and/or ferrihydrite had no stimulating effect on the overall emissions from the salt lakes. This suggests that Fe-metabolizing microorganisms do not contribute significantly to the formation at the field site investigated in this study and that the formation of the VOX compounds is probably mediated by halogenating enzymes such as chloroperoxoidases or methyltransferases. Furthermore, we demonstrated that Australian salt lakes such as Lake Whurr are suitable terrestrial analogues for past conditions on Mars. In addition to the similar mineralogy (presence of hematite and jarosite), Western Australian salt lakes are of particular interest because their pH values are less acidic than e.g. those from Rio Tinto (Spain), another terrestrial Mars analogue and thus are more similar to the conditions prevailing on Mars. Ribosomal tag pyrosequencing of DNA and RNA extracted from the hypersaline sediments of Lake Strawbridge revealed a high archaeal and bacterial diversity which was inversely correlated to the salinity of the sediments. By calculating RNA/DNA ratios we were able to identify taxonomic groups with a high protein synthesis potential and thereby a high potential activity. Surprisingly we observed several rare taxa such as Halomonas, Salinivibrio or the Marine benthic Group B with a high protein synthesis potential. Our results suggest that also rare taxa in hypersaline sediments are active and might therefore contribute to biogeochemical cycling and VOX formation in the sediments of Lake Strawbridge. In culture-dependent experiments with Sinorhizobium meliloti strain 1021 we were able to show that this common soil bacterium directly produces VOX when grown in a soil extract medium. Although we saw an increase in the smc01944 gene expression, which was suggested to encode for a chloroperoxidase, after the addition of H2O2, we did not see an increase in the VOX formation. Additionally no chloroperoxidase activity could be detected via an improved monochlorodimedone assay in which we quantified the halogenated product by LC-MS. Thus the exact formation mechanism of the observed VOX by S. meliloti strain 1021 remains to be elucidated. In microcosm experiments with soil from three soil horizons of the Schoenbuch forest we detected the formation of VOX such as chloroform and bromoform. To elucidate the genetic potential for a microbial halogen cycling in the Schoenbuch forest we applied a metagenomic approach on two replicate soil profiles using DNA extracted from the three topsoil horizons. We observed a so far unknown abundance and diversity of genes encoding for halogenating and dehalogenating enzymes in the investigated forest soil. The relative abundances of the most prominent genes for halogenases and dehalogenases were in the same order of magnitude as common nitrogen cycling genes (nosZ, nif-genes) or housekeeping genes such as alcohol dehydrogenases. The high abundance of genes and microorganisms involved in natural halogenation and dehalogenation reactions emphasizes the importance of microbial halogenation and dehalogenation reactions for the biogeochemical cycling of inorganic and organic forms of chloride/chlorine and bromide/bromine in soils.
Publications
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(2014) Predominance of biotic over abiotic formation of halogenated hydrocarbons in hypersaline sediments in Western Australia. Environmental Science and Technology, 48, 9170-9178
Ruecker, A., Weigold, P., Behrens, S., Jochmann, M., Laaks, J., Kappler, A.
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(2015) Formation of chloroform and tetrachloroethylene by Sinorhizobium meliloti strain 1021. Letters in Applied Microbiology, 61, 346-353
Weigold, P., Ruecker, A., Jochmann, M., Osorio Barajas, X., Lege, S., Zwiener, C., Kappler, A., Behrens, S.
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(2015) Halogenated hydrocarbon formation in a moderately acidic salt lake in Western Australia – role of abiotic and biotic processes. Environmental Chemistry, 12, 406-414
Ruecker, A., Weigold, P., Behrens, S., Jochmann, M., Osorio Barajas, X.L., Kappler, A.
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(2016) A metagenomic-based survey of microbial (de)halogenation potential in a German forest soil. Scientific Reports, 6, 28958
Weigold, P., El-Hadidi, M., Ruecker, A., Huson, D.H., Scholten, T., Jochmann, M., Kappler, A., Behrens, S.
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(2016) Geochemistry and mineralogy of Western Australian salt lake sediments: Implications for Meridiani Planum on Mars. Astrobiology, 16, 525-538
Ruecker, A., Schröder, C., Byrne, J., Weigold, P., Behrens, S., Kappler, A.
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(2016) Ribosomal tag pyrosequencing of DNA and RNA reveals 'rare' taxa with high protein synthesis potential in the sediment of a hypersaline lake in Western Australia. Geomicrobiology Journal, 33, 426-440
Weigold, P., Ruecker, A., Loesekann-Behrens, T., Kappler, A., Behrens, S.
