Transitory Microbial Habitat in the Hyperarid Atacama Desert

Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: a physico-chemical characterization of the soil habitability after an exceptional rain event, identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today's extreme hyperaridity. [Abstract copyright: Copyright © 2018 the Author(s). Published by PNAS.

Rates and potential mechanism of anaerobic nitrate-dependent microbial pyrite oxidation.

Pyrite (FeS2) is a major iron- and sulfur-containing mineral phase in the environment. Oxidation of pyrite by aerobic micro-organisms has been well investigated. However, the reactivity of pyrite under anoxic conditions is still an open question. In the present paper, we summarize field and laboratory data on this chemolithotrophic respiration process with nitrate as terminal electron acceptor. Geochemical and stable isotope field data indicate that this process is occurring. Laboratory studies are more ambiguous, but recent positive results provide evidence that anaerobic microbial pyrite oxidation can, in fact, occur with nitrate as electron acceptor

Anaerobic degradation of p-xylene by a sulfate-reducing enrichment culture.

A strictly anaerobic enrichment culture was obtained with p-xylene as organic substrate and sulfate as electron acceptor from an aquifer at a former gasworks plant contaminated with aromatic hydrocarbons. p-Xylene was completely oxidized to CO(2). The enrichment culture depended on Fe(II) in the medium as a scavenger of the produced sulfide. 4-Methylbenzylsuccinic acid and 4-methylphenylitaconic acid were identified in supernatants of cultures indicating that degradation of p-xylene was initiated by fumarate addition to one of the methyl groups. Therefore, p-xylene degradation probably proceeds analogously to toluene degradation by Thauera aromatica or anaerobic degradation pathways for o- and m-xylene

Anaerobic degradation of the aromatic hydrocarbon biphenyl by a sulfate-reducing enrichment culture.

The aromatic hydrocarbon biphenyl is a widely distributed environmental pollutant. Whereas the aerobic degradation of biphenyl has been extensively studied, knowledge of the anaerobic biphenyl-oxidizing bacteria and their biochemical degradation pathway is scarce. Here, we report on an enrichment culture that oxidized biphenyl completely to carbon dioxide under sulfate-reducing conditions. The biphenyl-degrading culture was dominated by two distinct bacterial species distantly affiliated with the Gram-positive genus Desulfotomaculum. Moreover, the enrichment culture has the ability to grow with benzene and a mixture of anthracene and phenanthrene as the sole source of carbon, but here the microbial community composition differed substantially from the biphenyl-grown culture. Biphenyl-4-carboxylic acid was identified as an intermediate in the biphenyl-degrading culture. Moreover, 4-fluorobiphenyl was converted cometabolically with biphenyl because in addition to the biphenyl-4-carboxylic acid, a compound identified as its fluorinated analog was observed. These findings are consistent with the general pattern in the anaerobic catabolism of many aromatic hydrocarbons where carboxylic acids are found to be central metabolites

Anaerobic degradation of non-substituted aromatic hydrocarbons.

Aromatic hydrocarbons are among the most prevalent organic pollutants in the environment. Their removal from contaminated systems is of great concern because of the high toxicity effect on living organisms including humans. Aerobic degradation of aromatic hydrocarbons has been intensively studied and is well understood. However, many aromatics end up in habitats devoid of molecular oxygen. Nevertheless, anaerobic degradation using alternative electron acceptors is much less investigated. Here, we review the recent literature and very early progress in the elucidation of anaerobic degradation of non-substituted monocyclic (i.e. benzene) and polycyclic aromatic hydrocarbons (PAH such as naphthalene and phenanthrene). A focus will be on benzene and naphthalene as model compounds. This review concerns the microbes involved, the biochemistry of the initial activation and subsequent enzyme reactions involved in the pathway

Enzymatic reactions in anaerobic 2-methylnaphthalene degradation by the sulphate-reducing enrichment culture N 47.

The upper pathway of anaerobic degradation of 2-methylnaphthalene was studied with a sulphate-reducing enrichment culture, which is able to grow with naphthalene or 2-methylnaphthalene as sole carbon source and electron donor. Anaerobic degradation of 2-methylnaphthalene is initiated by an addition of fumarate to the methyl-group producing the first intermediate, naphthyl-2-methyl-succinate. In a subsequent P-oxidation of the original methyl atom, the central metabolite 2-naphthoic acid is generated. In the following pathway, the aromatic ring system is reduced, cleaved, and finally oxidised to CO2. Here, we present two new enzymatic reactions of the 2-methylnaphthalene degradation pathway that were measured in crude cell extracts. All metabolites were identified with HPLC by co-elution with synthesised reference substances. The first enzyme, succinyl-CoA:naphthyl-2-methyl-succinate CoA-transferase, catalyses the activation of naphthyl-2-methyl-succinic acid to the corresponding CoA ester. The average specific activity of this enzyme was 19.6 nmol x min(-1) x mg of protein(-1). The CoA-transfer was not inhibited by sodium borohydride and only partially by hydroxylamine, indicating that this enzyme belongs to the family III of CoA-transferases like the corresponding enzyme in the anaerobic toluene degradation pathway. The product of this CoA-transfer reaction, naphthyl-2-methyl-succinyl-CoA is then oxidised in a reaction to naphthyl-2-methylene-succinyl-CoA by the enzyme naphthyl-2-methyl-suceinyt-CoA dehydrogenase. The specific activity of this enzyme was 0.115 nmol x min(-1) x mg of protein(-1). The enzymatic activity could only be detected using phenazine methosulphate as electron acceptor. No activity was observed with natural electron acceptors such as nicotinamide adenine dinucleotide or flavin adenine dinucleotide. The two novel reactions presented here demonstrate that the original methyl-group of 2-methylnaphthalene is oxidised to the carboxyl group of 2-naphthoic acid in the upper part of the anaerobic degradation pathway

Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria.

An anaerobic naphthalene-degrading culture (N49) was enriched with ferric iron as electron acceptor. A closed electron balance indicated the total oxidation of naphthalene to CO(2) . In all growing cultures, the concentration of the presumed central metabolite of naphthalene degradation, 2-naphthoic acid, increased concomitantly with growth. The first metabolite of anaerobic methylnaphthalene degradation, naphthyl-2-methyl-succinic acid, was not identified in culture supernatants, which does not support a methylation to methylnaphthalene as the initial activation reaction of naphthalene, but rather a carboxylation, as proposed for other naphthalene-degrading cultures. Substrate utilization tests revealed that the culture was able to grow on 1-methyl-naphthalene, 2-methyl-naphthalene, 1-naphthoic acid or 2-naphthoic acid, whereas it did not grow on 1-naphthol, 2-naphthol, anthracene, phenanthrene, indane and indene. Terminal restriction fragment length polymorphism and 16S rRNA gene sequence analyses revealed that the microbial community of the culture was dominated by one bacterial microorganism, which was closely related (99% 16S sequence similarity) to the major organism in the iron-reducing, benzene-degrading enrichment culture BF [ISME J (2007) 1: 643; Int J Syst Evol Microbiol (2010) 60: 686]. The phylogenetic classification supports a new candidate species and genus of Gram-positive spore-forming iron-reducers that can degrade non-substituted aromatic hydrocarbons. It furthermore indicates that Gram-positive microorganisms might also play an important role in anaerobic polycyclic aromatic hydrocarbon-degradation

Natural stable isotope fractionation for the assessment of hydrocarbon degradation.

In recent years, the use of compound specific isotope analysis (CSIA) to measure stable isotope fractionation developed into one of the most important tools for assessing biodegradation of aromatic hydrocarbons in contaminated groundwater. Biodegradation reactions are often accompanied by shifts in the stable isotope ratios of the naturally abundances of e.g., 13C/12C, 2H/1H, or other elements of the compound of interest. This isotope fractionation is measured in the residual substrate fraction sampled from monitoring wells by means of CSIA. If laboratory degradation experiments have been performed to obtain stable isotope fractionation factors for a given compound and reaction one can use the Rayleigh equation to calculate the extent of biodegradation in the environment. The big advantage of the stable isotope fractionation approach is that one can even quantify the extent of biodegradation in extremely complex matrices such as aquifers. Several field studies successfully showed astonishing accuracy of the method to determine biodegradation rates on contaminated field sites. Nowadays, stable isotope tools are widely accepted by authorities as a reliable tool to prove biodegradation in natural attenuation. Here, we give a brief introduction how to use CSIA for assessing stable isotope fractionation of aromatic hydrocarbons together with a few selected successful examples of application