Microbial synthesis and transformation of inorganic and organic chlorine compounds

Organic and inorganic chlorine compounds are formed by a broad range of natural geochemical, photochemical and biological processes. In addition, chlorine compounds are produced in large quantities for industrial, agricultural and pharmaceutical purposes, which has led to widespread environmental pollution. Abiotic transformations and microbial metabolism of inorganic and organic chlorine compounds combined with human activities constitute the chlorine cycle on Earth. Naturally occurring organochlorines compounds are synthesized and transformed by diverse groups of (micro)organisms in the presence or absence of oxygen. In turn, anthropogenic chlorine contaminants may be degraded under natural or stimulated conditions. Here, we review phylogeny, biochemistry and ecology of microorganisms mediating chlorination and dechlorination processes. In addition, the co-occurrence and potential interdependency of catabolic and anabolic transformations of natural and synthetic chlorine compounds are discussed for selected microorganisms and particular ecosystems.The authors thank METAEXPLORE, funded by the European Union Seventh Framework Program (Grant No. 222625), BEBASIC-FES funds from the Dutch Ministry of Economic Affairs (Projects F07.001.05 and F08.004.01), Shell Global Solutions International BV, the ERC Advanced grant “Novel Anaerobes” (Project 323009), the SIAM Gravitation grant “Microbes for Health and the Environment” (Project 024.002.002) of the Netherlands Ministry of Education, Culture and Science, and the Netherlands Science Foundation (NWO) for funding.info:eu-repo/semantics/publishedVersio

Perchlorate and chlorate reduction by the Crenarchaeon Aeropyrum pernix and two thermophilic Firmicutes

This study reports the ability of one hyperthermophile and two thermophilic microorganisms to grow anaerobically by the reduction of chlorate and perchlorate. Physiological, genomic and proteome analyses suggest that the Crenarchaeon Aeropyrum pernix reduces perchlorate with a periplasmic enzyme related to nitrate reductases, but that it lacks a functional chlorite-disproportionating enzyme (Cld) to complete the pathway. A. pernix, previously described as a strictly aerobic microorganism, seems to rely on the chemical reactivity of reduced sulfur compounds with chlorite, a mechanism previously reported for perchlorate-reducing Archaeoglobus fulgidus. The chemical oxidation of thiosulfate (in excessive amounts present in the medium) and the reduction of chlorite result in the release of sulfate and chloride, which are the products of a biotic-abiotic perchlorate reduction pathway in A. pernix. The apparent absence of Cld in two other perchlorate-reducing microorganisms, Carboxydothermus hydrogenoformans and Moorella glycerini strain NMP, and their dependence on sulfide for perchlorate reduction is consistent with observations made on A. fulgidus. Our findings suggest that microbial perchlorate reduction at high temperature differs notably from the physiology of perchlorate- and chlorate-reducing mesophiles and that it is characterized by the lack of a chlorite dismutase and is enabled by a combination of biotic and abiotic reactions.This research was financially supported by Shell Global Solutions International BV. Research of AJMS is supported by ERC grant (project 323009) and the Gravitation grant (project 024.002.002) of the Netherlands Ministry of Education, Culture and Science and the Netherlands Science Foundation (NWO). Sequencing data for strain NMP have been submitted to the European Nucleotide Archive (ENA) under accession number PRJEB8377. Mass spectrometry proteomics data and database search results have been deposited to the ProteomeXchange Consortium (Vizcaino et al., 2014) via the PRIDE partner repository with the dataset identifier PXD001683 and DOI 0.6019/PXD001683

Archaeal (per)chlorate reduction at high temperature: an interplay of biotic and abiotic reactions

Perchlorate and chlorate anions [(per)chlorate] exist in the environment from natural and anthropogenic sources, where they can serve as electron acceptors for bacteria. We performed growth experiments combined with genomic and proteomic analyses of the hyperthermophile Archaeoglobus fulgidus that show (per)chlorate reduction also extends into the archaeal domain of life. The (per)chlorate reduction pathway in A. fulgidus relies on molybdo-enzymes that have similarity with bacterial enzymes; however, chlorite is not enzymatically split into chloride and oxygen. Evidence suggests that it is eliminated by an interplay of abiotic and biotic redox reactions involving sulfur compounds. Biological (per)chlorate reduction by ancient archaea at high temperature may have prevented accumulation of perchlorate in early terrestrial environments and consequently given rise to oxidizing conditions on Earth before the rise of oxygenic photosynthesis.We thank D. Frigo and M. Golombok for critically reviewing the manuscript and Shell Global Solutions International BV for financial support. A.J.M.S. acknowledges the support of the Technology Foundation STW (project 08053) and the Chemical Sciences division CW (project 700.55.343) of the Netherlands Science Foundation (NWO). The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium with the data set identifier PXD000137 and digital object identifier 10.6019/PXD000137. The experiments were conceived by M. G. L., A.J.M.S., and B. P. L. Growth experiments, enzyme activity measurements and chemical analyses were conducted by M. G. L. The proteome analysis was performed by M. W. H. P. Data processing and interpretation of the proteome analysis was done by P.J.S. and M. G. L. The manuscript was written by M. G. L. with input from all other authors

Bacterial glycerol oxidation coupled to sulfate reduction at neutral and acidic pH

Glycerol is a main co-product of biodiesel production. Crude glycerol may serve as a cheap and attractive substrate in biotechnological applications, e.g. for the production of valuable chemicals or as an electron donor for reduction processes. In this work, sulfate reduction with glycerol was studied at neutral and acidic pH using bioreactor sludge samples and Tinto River sediments as a source of inoculum, respectively. Communities of sulfate-reducing bacteria (SRB) and fermentative bacteria were co-enriched at both pH values. Molecular analyses revealed that sequences belonging to Desulfomicrobium genus were dominant in the cultures enriched at pH 7, while Desulfosporosinus sequences dominated in the culture enriched at pH 4. Glycerol conversion was coupled to sulfate reduction, but the substrate was incompletely oxidized to acetate in the neutrophilic enrichments, and acetate, lactate, and 1,3-propanediol under low pH conditions. Two strains belonging to Desulfomicrobium and Proteiniphilum genera were isolated from the neutrophilic enrichments, but the first isolate was not able to use glycerol, which suggests a syntrophic relationship between glycerol-degrading fermentative bacteria and SRB. A Clostridium strain able to grow with glycerol was isolated from the low pH enrichment. Our data indicate that glycerol promotes the growth of sulfate-reducing communities to form sulfide, which can be used to precipitate and recover heavy metals.The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Spanish Ministerio de Ciencia e Innovación (grant CTM2009-10521), the European Research Council (project 323009) and the graduate school WIMEK SENSE for support. The research was part of the PhD program of the Northeast Brazil Biotechnology Network (RENORBIO).info:eu-repo/semantics/publishedVersio