Sulfur-Dependent Microbial Lifestyles: Deceptively Flexible Roles for Biochemically Versatile Enzymes Crane 141

Available online at www.sciencedirect.com ScienceDirect Sulfur-dependent microbial lifestyles: deceptively flexible roles for biochemically versatile enzymes Edward J Crane III Abstract of sulfur in a manner similar to the utilization of starch granules by yeast [1]. In a series of elegant experiments A wide group of microbes are able to “make a living” on Earth originally designed to confirm the idea that individual by basing their energetic metabolism on inorganic sulfur species of bacteria existed that exhibited defined charac- compounds. Because of their range of stable redox states, teristics (known as monomorphism) Winogradsky not only sulfur and inorganic sulfur compounds can be utilized as either provided support that the microbial community was made oxidants or reductants in a diverse array of energy-conserving up of a diverse array of defined species, he also demon- reactions. In this review the major enzymes and basic strated the first known case of chemolithotrophy, at the chemistry of sulfur-based respiration and chemolithotrophy are same time establishing the fields of geomicrobiology and outlined. The reversibility and versatility of these enzymes, microbial ecology [3]. The importance of the microbes and however, means that they can often be used in multiple ways, enzymes capable of sulfur-based chemolithoautotrophy and several cases are discussed in which enzymes which are and photoautotrophy (using sulfur compounds as energy considered to be hallmarks of a particular respiratory or and/or electron sources, respectively, in theoxidative direc- lithotrophic process have been found to be used in other, often tion) and sulfur-based respiration (in the reductive direc- opposing, metabolic processes. These results emphasize the tion) on the formation and maintenance of the biosphere importance of taking into account the geochemistry, and geosphere is only beginning to be understood [4]. The biochemistry and microbiology of an organism and/or biochemical foundations for these reactions are reasonably environment when trying to interpret the function of a particular well understood, and monoculture and community culture sulfur-dependent redox enzyme. techniques have been used to characterize microbes Address responsible for the reactions. Department of Biology, Pomona College, 645 N. College Ave., Claremont, CA 91711, USA Sulfur-dependent microbial lifestyle Corresponding author: Crane, Edward J ([email protected]) With the exponential development of molecular techniques and cataloging of enzymes and pathways (in data- Current Opinion in Chemical Biology 2019, 49:139–145 bases such as KEGG [5], etc.), it has become practically This review comes from a themed issue on Bioinorganic chemistry possible to detect many or most of the genes, and, therefore, potential enzymes and pathways/microbial Edited by Kyle M Lancaster functions, present in an environmental sample (e.g. For a complete overview see the Issue and the Editorial Ref. [6]). Through further analysis, it is possible to assign Available online 8th February 2019 those genes to organisms, and even to assemble genomes https://doi.org/10.1016/j.cbpa.2018.12.015 of organisms present (e.g. Refs. [7 ,8,9 ,10]). The result of 1367-5931/ã 2019 Elsevier Ltd. All rights reserved. this is that it now appears technically possible to deter- mine the biochemical pathways present in an environmental sample, and, therefore, what types of sulfur chemistry will be performed by individual microbes or communities of organisms. Many caveats should be considered when trying to infer which functional pathways and metabolisms are present in an organism or environ- “ . the sulfur in these organisms is the sole respi- ment through these types of analyses. One of the most ratory source, and in that sense plays the same role as significant considerations is that many of the enzymes that of carbohydrate in other organisms . [1] . that are considered to be hallmarks of certain pathways A completesynthesis oforganic material bytheaction are often functional in either the reverse direction or in of living organisms has been accomplished on our other pathways. As an example, the dsrAB genes, which planet independent of solar energy [2].” are usually considered to be the hallmark of sulfate- Sergei Winogradsky respiring microbes, can be used in the reverse direction, and are often found in non-sulfate-respiring organisms, as Introduction discussed below. This means that the presence of genes In 1887, the incomparable Winogradsky noted that cells of in a genome or metagenome is not a guarantee that a the (relatively) large bacterium Beggiatoa utilized granules certain microbial metabolism predominates, or is even www.sciencedirect.com Current Opinion in Chemical Biology 2019, 49:139–145 140 Bioinorganic chemistry significantly present, in a given sample. The observation reactivity, and on the basis of these differences, six also emphasizes that the finding of genes, transcripts or different groups of the enzyme have been proposed proteins in a sample should always be considered in the [19,20]. In humans (and eukaryotes in general), it has context of the other metabolites and substrates, proteins, been proposed to be involved in sulfide signaling pro- genes and microbes present in a sample, as well the geo or cesses and maintaining redox balance in the mitochon- biochemical context of the sample. While the range of dria, and has been proposed to play a similar role in some ‘-omic’ techniques and systems biology are complement- bacteria [21,22]. SQR is in the same large family as the ing our chemical understanding of sulfur-based chemo- Nsr/CoADR/Npsrs discussed below, and has an active lithoautotrophy and respiration, careful enzymology, geo- site that utilizes both an FAD and a redox-active cysteine chemistry and microbiology are still necessary to provide pair. The SQRs differ from other members of this family; proof of the systems in operation in microbes and the however, in that they are periplasm-facing peripheral or environment (e.g. see Ref. [11]). integral membrane proteins, and they do not utilize NAD (P)H, and, depending on the reaction direction, use either This review will focus on sulfur cycling in the environ- a range of electron donors such as cytochrome c to transfer ment via dissimilatory processes and chemolithoautotro- electrons to their bound quinone, or sulfide. From a phy, emphasizing cases in which enzymes normally con- geochemical perspective, SQR is considered to function sidered to be ‘hallmarks’ for a given inorganic sulfur in vivo in sulfide oxidation; however, there is transcrip- transformation that have been observed to catalyze other tomic evidence that it participates in the reductive direc- processes. While the focus on this review is somewhat tion as well [23 ]. ‘gene-heavy,’ the reason for the difficulty in assigning function discussed here is a very chemical one: the Sulfur-based respiration — sulfate reduction reversibility of many of the redox reactions involved, as In terms of the respiratory or reductive pathways of sulfur well as the intersections of the chemistry of dissimilatory compounds, especially in terms of the magnitude of effect (i.e. energy conserving), assimilatory (for cell building), on the geosphere, the dissimilatory sulfate reduction 2À À 2À detoxification and the somewhat nebulous redox balanc- pathway predominates (SO4 + 8e ! S , via adeno- 0 ing reactions in the cell means that the same reaction can sine-5 -phosphosulfate (APS) and sulfite intermediates) serve many different functions. When combined with the [24]. As an example, it is responsible for half of the modular nature of the catalysts that nature has provided mineralization (i.e. conversion to inorganic carbon) that [12], the biochemistry becomes quite difficult to occurs at the sea floor [25]. The hallmark for sulfate disentangle. reduction is generally considered to be the dsrAB sulfite reductase, although the transfer of a sulfane sulfur by Sulfur-based chemolithoautotrophy DsrC is likely to be the rate-limiting step for the reaction Biochemical pathways for sulfur-dependent chemo- in the cell [26], with a protein trisulfide linking DsrAB to lithoautotrophy (essentially, ‘eating’ sulfide or sulfur) DsrC [27,28]. The dsrAB genes code a tetrasiroheme- are highly diverse, in terms of phylogeny, subcellular containing heterotetrameric (a2b2) sulfite dehydrogenase 2À À location of enzymes and intermediates, and the inter- (SO3 + 6e $ H2S + 3H2O), and while it is clear that mediates involved, making a brief review of the subject dsrAB genes that code for the reductive or oxidative difficult [13]. As a generalization, the process involves the reactions are usually phylogenetically distinct [29], it 2À oxidation of sulfide or elemental sulfur to sulfate (S or was recently found that genes predicted to code for 0 2À S ! SO4 ), an exergonic process that allows for carbon reductive DsrABs were implicated in sulfide oxidation fixation under the right conditions [14,15]. The predomi- [30 ]. Other enzymes distinct from the DsrABs have also nant genes that allow for autotrophic growth on sulfide are been found to catalyze the dissimilatory reduction of the genes of the sox clusters; however, in keeping with the sulfite, such as the octaheme SirA from the sulfite (but theme of this article, the presence of sox genes is no not sulfate) reducing Shewanella oneidensis MR-1 [31]. guarantee an organism is capable of sulfur/-ide dependent chemolithoautotrophic metabolism, and sox genes are As an example

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