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Sulfate Transporters in Dissimilatory Sulfate Reducing Microorganisms: a Comparative Genomics Analysis

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Sulfate Transporters in Dissimilatory Sulfate Reducing Microorganisms: a Comparative Genomics Analysis fmicb-09-00309 February 28, 2018 Time: 16:16 # 1 REVIEW published: 02 March 2018 doi: 10.3389/fmicb.2018.00309 Sulfate Transporters in Dissimilatory Sulfate Reducing Microorganisms: A Comparative Genomics Analysis Angeliki Marietou*, Hans Røy, Bo B. Jørgensen and Kasper U. Kjeldsen Center for Geomicrobiology, Department of Bioscience, Aarhus University, Aarhus, Denmark The first step in the sulfate reduction pathway is the transport of sulfate across the cell membrane. This uptake has a major effect on sulfate reduction rates. Much of the information available on sulfate transport was obtained by studies on assimilatory sulfate reduction, where sulfate transporters were identified among several types of protein families. Despite our growing knowledge on the physiology of dissimilatory sulfate- reducing microorganisms (SRM) there are no studies identifying the proteins involved in sulfate uptake in members of this ecologically important group of anaerobes. We Edited by: surveyed the complete genomes of 44 sulfate-reducing bacteria and archaea across Alexander Loy, six phyla and identified putative sulfate transporter encoding genes from four out of the University of Vienna, Austria five surveyed protein families based on homology. We did not find evidence that ABC- Reviewed by: Michael Pester, type transporters (SulT) are involved in the uptake of sulfate in SRM. We speculate that Deutsche Sammlung von members of the CysP sulfate transporters could play a key role in the uptake of sulfate in Mikroorganismen und Zellkulturen (DSMZ), Germany thermophilic SRM. Putative CysZ-type sulfate transporters were present in all genomes Karthik Anantharaman, examined suggesting that this overlooked group of sulfate transporters might play a role University of Wisconsin–Madison, in sulfate transport in dissimilatory sulfate reducers alongside SulP. Our in silico analysis United States highlights several targets for further molecular studies in order to understand this key *Correspondence: Angeliki Marietou step in the metabolism of SRMs. [email protected] Keywords: sulfate transporter, sulfate-reducing microorganisms, SulP, CysP, CysZ, DASS Specialty section: This article was submitted to Evolutionary and Genomic INTRODUCTION Microbiology, a section of the journal Dissimilatory sulfate reduction is a key metabolic process in anoxic environments. It is catalyzed Frontiers in Microbiology by sulfate-reducing microorganisms (SRM), which encompass a diverse group of bacteria and Received: 03 December 2017 archaea spanning several phylogenetic lineages (Müller et al., 2015). SRM use sulfate as terminal Accepted: 09 February 2018 electron acceptor for the oxidation of organic electron donors or hydrogen, thereby producing Published: 02 March 2018 sulfide, which they release back to the environment (dissimilatory sulfate reduction). Sulfate can Citation: also be reduced and assimilated for the synthesis of cell material whereby the produced sulfide is Marietou A, Røy H, Jørgensen BB incorporated into sulfur-containing compounds like cysteine (assimilatory sulfate reduction). The and Kjeldsen KU (2018) Sulfate initial two steps of sulfate metabolism are similar in both dissimilatory and assimilatory pathways Transporters in Dissimilatory Sulfate of sulfate reduction. The sulfate ion is first transported through the hydrophobic membrane Reducing Microorganisms: A Comparative Genomics Analysis. into the cytoplasm and then activated with ATP forming the intermediate APS (adenosine-5- Front. Microbiol. 9:309. phosphosulfate). Since the sulfate ion cannot enter the cell by passive diffusion, a specialized doi: 10.3389/fmicb.2018.00309 transport system is required by all sulfate-utilizing microorganisms. Frontiers in Microbiology| www.frontiersin.org 1 March 2018| Volume 9| Article 309 fmicb-09-00309 February 28, 2018 Time: 16:16 # 2 Marietou et al. Sulfate Transporters in Sulfate Reducing Microorganisms Despite the growing knowledge on the physiology of the pH gradient across the membrane (Cypionka, 1989, 1995). dissimilatory sulfate reduction most of the information regarding At neutral external pH the average 1pH is 0.5 and if we the sulfate transport proteins involved in the dissimilatory assume the electrical potential to be −150 mV,then electroneutral pathway has been adopted from the assimilatory pathway symport with two cations would result in 10-fold accumulation literature. There are five major families of sulfate transporter (low affinity transport), while electrogenic symport with three proteins that have been previously identified in assimilatory cations would allow 10,000-fold accumulation of sulfate (high sulfate-reducing prokaryotic and eukaryotic organisms (Kertesz, affinity transport) (Cypionka, 1989). A 20,000-fold accumulation 2001; Piłsyk and Paszewski, 2009; Aguilar-Barajas et al., 2011): was reported at external sulfate concentrations of 0.1 mM in (1) The SulT sulfate transporters [Transporter Classification Desulfovibrio salexigens (Kreke and Cypionka, 1994). DataBase (TCDB) 3.A.1.6] are members of the ATP-Binding High accumulation of sulfate was only observed under sulfate- Cassette (ABC) (TCDB 3.A.1) superfamily of proteins that limitation (less than 1 mM of sulfate) suggesting regulation transport a wide range of molecules but also participate in of the high affinity transport system at the molecular level several cellular processes and have been extensively characterized (Stahlmann et al., 1991). A low affinity system operates when in Escherichia coli and Salmonella sp. (Dassa and Bouige, sulfate concentration is 1 mM or higher; the high affinity system 2001; Saier et al., 2006). (2) The SulP sulfate transporters is then switched off in order to save energy and prevent an over- (TCDB 2.A.53) which are part of the Amino acid-Polyamine- accumulation of sulfate inside the cell (Stahlmann et al., 1991). organoCation (APC) superfamily of proteins (TCDB 2.A.3) that The marine sulfate reducer Desulfobacterium autotrophicum function as solute:cation and solute:solute antiporters and have switched from low affinity to high affinity sulfate reduction when been characterized in Mycobacterium tuberculosis (Saier, 2000; the concentration of sulfate dropped below 500 mM with a Zolotarev et al., 2008). (3) The CysP sulfate transporters (TCDB concomitant change in the expression of genes encoding putative 2.A.20.4.1), which are members of the inorganic Phosphate sulfate transport proteins from the SulP and DASS families Transporter (TCDB 2.A.20) family (PiT) that function mainly (Tarpgaard et al., 2017). as inorganic phosphate or sulfate transporters with either HC With the help of comparative genomics this review aimed to or NaC symport and have been characterized in Bacillus subtilis (i) identify putative homologs of sulfate transporters in SRM, (Saier et al., 1999; Mansilla and de Mendoza, 2000). (4) The DASS (ii) determine their taxonomic distribution and their genomic (Divalent Anion: NaC Symporter) sulfate transporters (TCDB context and hereby infer their putative function as sulfate 2.A.47) which belong to the Ion Transporter (IT) superfamily of transporters, and (iii) provide a reference roadmap of putative secondary carriers of cationic and anionic compounds have been sulfate transporters in SRM for further explorations. characterized in Rhodobacter capsulatum (Prakash et al., 2003; Gisin et al., 2010). (5) The CysZ sulfate transporters, members of the TSUP (Toluene Sulfonate Uptake Permease) family (TCDB: ANALYTICAL APPROACH 2.A.102). The TSUP transporters form a ubiquitous and diverse family of transmembrane proteins that are poorly characterized Protein Identification but predicted to be involved in the transport of sulfur-based The IMG/MER online database (Markowitz et al., 2011) molecules (Shlykov et al., 2012). was searched (accessed on 15 December 2015) using the Sulfate concentrations vary in the environment from 28 mM following PFAM models for transporter families with members in seawater to a few micromolar in freshwater environments known to transport sulfate across the cytoplasmic membrane and in the gastrointestinal tract of animals. Microorganisms have using the default search parameters of the Function Search developed dual kinetic approaches to transport sulfate efficiently option: PFAM00916 (SulP family), PFAM00939 (DASS family), at varying concentrations. Concurrent high and low affinity PFAM01384 (CysP family). Since there was no PFAM model sulfate reduction was reported in marine sediments (Tarpgaard available for the CysZ-family of transporters the transporter et al., 2011). At high sulfate concentrations, sulfate is transported classification number TC9.A.29 for the TSUP protein family into the cell using an electroneutral system driven by the pH was used instead for the Function Search option at the gradient across the membrane, where two cations are symported IMG/MER database (Saier et al., 2013). For the SulT family per sulfate (Cypionka, 1989). When the sulfate concentration of transporters the IMG/MER database was searched using in the environment is extremely low, an electrogenic sulfate TIGRFAM models (TIGR00968, TIGR00969, and TIGR00971) transport system is used that symports three cations per sulfate and blastp (E-value cut-off: 1e-5) using the SulT family molecule (Cypionka, 1989). The steady state accumulation of sulfate permease protein sequence from Salmonella enterica LT2 sulfate in symport with HC or NaC can be described by the (AAL22903) as query. The genomes selected for each search equation: query were at the “Finished”
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