9.B.102 The YedE/YeeE (YeeE) Family

The YeeE family (also called the COG2392 or DUF395 family) consists of numerous putative transport proteins of from 4 to 10 TMSs (G Madrigal, P Kabran and M Saier, unpublished observations). Some of these (i.e PmpA and PmpB, both of 4 TMSs) may function together as a heterodimeric transporter. In some cases, two YeeE homologues are encoded in a single operon with a member of the TSUP family e.g., PmpC (2.A.102.4.2; Gristwood et al., 2011). Some evidence suggests that some of these proteins may play a role in sulfur and/or selenium metabolism (Lin et al. 2015). The smaller proteins (4 - 6 TMSs) have one of two conserved, related motifs, A or B, while the larger proteins (9 - 10 TMSs) have both in either of the two possible orders, A - B or B - A within two repeat segemnts of 5 TMSs (unpublished results). 



This family belongs to the .

 

References:

Bagchi, A. (2013). Structural analyses of the permease like protein SoxT: a member of the sulfur compound metabolizing sox operon. Gene 521: 207-210.

Dahl, J.U., C. Radon, M. Bühning, M. Nimtz, L.I. Leichert, Y. Denis, C. Jourlin-Castelli, C. Iobbi-Nivol, V. Méjean, and S. Leimkühler. (2013). The sulfur carrier protein TusA has a pleiotropic role in Escherichia coli that also affects molybdenum cofactor biosynthesis. J. Biol. Chem. 288: 5426-5442.

Darshan, N. and H.K. Manonmani. (2015). Prodigiosin and its potential applications. J Food Sci Technol 52: 5393-5407.

Gristwood, T., M.B. McNeil, J.S. Clulow, G.P. Salmond, and P.C. Fineran. (2011). PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J. Bacteriol. 193: 1076-1085.

Higgins, K.A., H. Peng, J.L. Luebke, F.M. Chang, and D.P. Giedroc. (2015). Conformational analysis and chemical reactivity of the multidomain sulfurtransferase, Staphylococcus aureus CstA. Biochemistry 54: 2385-2398.

Joshi, R. and B.B. McSpadden Gardener. (2006). Identification and Characterization of Novel Genetic Markers Associated with Biological Control Activities in Bacillus subtilis. Phytopathology 96: 145-154.

Lahiri, C., S. Mandal, W. Ghosh, B. Dam, and P. Roy. (2006). A novel gene cluster soxSRT is essential for the chemolithotrophic oxidation of thiosulfate and tetrathionate by Pseudaminobacter salicylatoxidans KCT001. Curr. Microbiol. 52: 267-273.

Lee, J., S. Ghosh, and M.H. Saier, Jr. (2017). Comparative genomic analyses of transport proteins encoded within the red algae Chondrus crispus, Galdieria sulphuraria, and Cyanidioschyzon merolae(11). J Phycol 53: 503-521.

Lee, K.Y., J.H. Kim, K.Y. Lee, J. Lee, I. Lee, Y.J. Bae, and B.J. Lee. (2013). Structural characterization of HP1264 reveals a novel fold for the flavin mononucleotide binding protein. Biochemistry 52: 1583-1593.

Lin, J., T. Peng, L. Jiang, J.Z. Ni, Q. Liu, L. Chen, and Y. Zhang. (2015). Comparative genomics reveals new candidate genes involved in selenium metabolism in prokaryotes. Genome Biol Evol 7: 664-676.

Salazar, J.K., K. Deng, M.L. Tortorello, M.T. Brandl, H. Wang, and W. Zhang. (2013). Genes ycfR, sirA and yigG contribute to the surface attachment of Salmonella enterica Typhimurium and Saintpaul to fresh produce. PLoS One 8: e57272.

Shlykov, M.A., W.H. Zheng, J.S. Chen, and M.H. Saier, Jr. (2012). Bioinformatic characterization of the 4-Toluene Sulfonate Uptake Permease (TSUP) family of transmembrane proteins. Biochim. Biophys. Acta. 1818: 703-717.

Stockdreher, Y., M. Sturm, M. Josten, H.G. Sahl, N. Dobler, R. Zigann, and C. Dahl. (2014). New proteins involved in sulfur trafficking in the cytoplasm of Allochromatium vinosum. J. Biol. Chem. 289: 12390-12403.

Teplitski, M., A. Al-Agely, and B.M. Ahmer. (2006). Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium. Microbiology 152: 3411-3424.

Examples:

TC#NameOrganismal TypeExample
9.B.102.1.1

YedE; 401aas; 10 TMSs (Gristwood et al., 2011).  Evidence suggests it may play a role in selenium transport (Lin et al. 2015).

Proteobacteria

YedE of E. coli (P31064)

 
9.B.102.1.10

YeeE homologue of 409 aas

Crenarchaea

YeeE homologue of Sulfolobus solfataricus

 
9.B.102.1.11

YeeE homologue of 329 aas and 10 TMSs

Fungi

YeeE homologue of Metarhizobium anisopliae

 
9.B.102.1.12

YeeE/YedE protein with 9 TMSs and a C-terminal SirA/YedF/YeeD/YvrY domain of about 100 aas. The hydrophilic SirA α/β sandwich domain has been suggested to be involved in surface attachement and biofilm formation in enteric bacteria (Teplitski et al. 2006; Salazar et al. 2013). However, SirA/TusA/YhhP proteins bind FMN, catalyze sulfur transfer, and are important for sulfur oxidation, tRNA thiomodification and molybdenum cofactor biosynthesis (Dahl et al. 2013; Lee et al. 2013; Higgins et al. 2015)  Homologues have been shown to bind sulfur via a cysteyl residue, and growth on sullfide in sufur oxidation bacteria requires such a homologue (Stockdreher et al. 2014). Genes encoding homologues of YeeD are often found sandwiched in between the two genes encoding half sized YeeE homologues of 4 or 5 TMSs.

Actinobacteria

YeeE homologue of Corynebacterium efficiens

 
9.B.102.1.13

Uncharacterized YeeE homologue of 305 aas

Spirochaetes

YeeE homologue of Turneriella parva

 
9.B.102.1.14

YedE homologue of 349 aas and 10 TMSs

Spirochaetes

YedE of Treponema pedis

 
9.B.102.1.15

YeeE homologue of 425 aas and 10 TMSs

YeeE homologue of Erysipelothrix rhusiopathiae

 
9.B.102.1.16

Uncharacterized protein of 333 aas and 9 TMSs

UP of Pseudothermotoga thermarum

 
9.B.102.1.17

Uncharacterized protein of 360 aas and 10 TMSs

UP of Pyrobaculum oguniense

 
9.B.102.1.18

Uncharacterized protein of 167 aas and 4 TMSs

UP of Caldithrix abyssi

 
9.B.102.1.19

YeeE homologue of 187 aas and 5 TMSs

YeeE of Pedobacter heparinus

 
9.B.102.1.2

YeeE/UPF0394 family; DUF395 (352aas; 9 or 10 TMSs)

Bacteria

YeeE of E. coli (P33015)

 
9.B.102.1.20

YeeE homologue of 157 aas and 4 TMSs

YeeE homologue of Methanocaldococcus fervens  (Methanococcus fervens)

 
9.B.102.1.21

Uncharacterized protein of 285 aas and 8 TMSs.

UP of Photobacterium profundum

 
9.B.102.1.22

Uncharacteerized protein of 458 aas and 10 TMSs

UP of Thermoplasmatales archaeon I-plasma

 
9.B.102.1.3

Uncharacterized protein of 363 aas and 10 TMSs (Cluster 2).

Slime molds

UP of Dictyostelium discoideum

 
9.B.102.1.4

Putative permease of 228 aas and 6 TMSs (Cluster 3).

Firmicutes

PP of Clostridium tetani

 
9.B.102.1.5

Uncharacterized protein of 371 aas and 10 TMSs (Cluster 4).

Proteobacteria

UP of Geobacter metallireducens

 
9.B.102.1.6

Uncharacterized protein of 402 aas (cluster 5)

Euryarchaea

UP of Halorubrum lacusprofundi

 
9.B.102.1.7

YeeE homologue of 172 aas.

Archaea

YeeE homologue of Methanosaeta harundinacea

 
9.B.102.1.8

YeeE homologue of 398 aas and 10 TMSs.

Archaea

YeeE homologue of Desulfonatonospira thiodismutans

 
9.B.102.1.9

YeeE homologue of 422 aas and 11 TMSs.

Euryarchaea

YeeE homologue of Thermoplasma acidophilum

 
Examples:

TC#NameOrganismal TypeExample
9.B.102.2.1

Putative MFS permease (384aa; 10-12 TMSs)

Bacteria

Putative MFS permease of Thiomonas sp 3As (D6CN48)

 
9.B.102.2.2

YeeE homologue of 375 aas and 9 TMSs.

Proteobacteria

YeeE homologue of Bordetella avium

 
9.B.102.2.3

YeeE homologue of 396 aas and 10 TMSs

YeeE of Variovorax paradoxus

 
9.B.102.2.4

Uncharacterized protein of 403 aas and 12 TMSs

UP of Thalassospira profundimaris

 
9.B.102.2.5

YeeE homologue of 122 aas and 4 TMSs

YeeE of Candidatus Entotheonella sp. TSY2

 
Examples:

TC#NameOrganismal TypeExample
9.B.102.3.1

SoxT, a putative permease encoded in an operon (soxSRT) concerned with the oxidation of both thiosulfate and tetrathionate (Lahiri et al., 2006). The putative transprter is 362aas in length with 10 putative TMSs in an apparent 2+2+2+2+2 arrangement.  SoxT has been modeled after LacY with predictions of substrate binding (Bagchi 2013).

Bacteria

SoxT of Pseudoaminobacter salicylatoxidans (Q5ZQN6)

 
9.B.102.3.2

Uncharacterized protein of 423 aas and 9 TMSs (Cluster 1).

Proteobacteria

UP of Alkalilimnicola ehrlichei

 
9.B.102.3.3

Membrane protein of 371 aas and 9 TMSs

Proteobacteria

Membrane protein of Ramlibacter tataouinensis

 
9.B.102.3.4

Uncharacterized protein of 383 aas and 9 TMSs

UP of Aurantimonas manganoxydans

 
9.B.102.3.5

YeeE homoogue of 357 aas and 9 TMSs

YeeE of Ruegeria pomeroyi (Silicibacter pomeroyi)

 
Examples:

TC#NameOrganismal TypeExample
9.B.102.4.1

Rhodanese domain-containing protein (RCP) (647aas; The 6 N-terminal TMSs are distantly related to YeeE (TC#9.B.102.1.2))

Bacteria

RCP of Syntrophobacter fumaroxidans (A0LFK9)

 
9.B.102.4.2

YeeE homologue of 218 aas

Proteobacteria

YeeE homologue of Anaeromyxobacter dehalogenans

 
9.B.102.4.3

YeeE homologue of 185 aas

Proteobacteria

YeeE homologue of Geobacter sulfurreducens

 
9.B.102.4.4

YeeE-Rhodanese fusion protein of 419 aas

Verrucomicrobia

fusion protein of Opitutus terrae

 
9.B.102.4.5

YeeE homologue of 175 aas and 5 TMSs

Firmicutes

YeeE homologue of Sporomusa ovata

 
Examples:

TC#NameOrganismal TypeExample
9.B.102.5.1

Putative permease of 147 aas and 4 TMSs.

Bacteria

Putative permease of Thiomonas sp. 3As (D6CUL1)

 
9.B.102.5.2

Putative permease subunit of 142 aas and 4 TMSs, PmpA.  The N- and C-termni are predicted to be outside.  It belongs to the Duf395/COG2391 family.  Its structural gene, pmpA, is adjacent to pmpB (TC# 9.B.102.5.5) which encodes another small 4 TMS protein of opposite orientation in the membrane.  These genes and pmpC, encoding a transporter of the TSUP family (2.A.102) that might function in sulfur or selenium metabolism (Lin et al. 2015), are localized in a gene cluster concerned with prodigiosin (red pigment (Darshan and Manonmani 2015)) production (Gristwood et al. 2011).  Hence, PmpA/PmpB might export prodigiosin, but no direct evidence is available to support such a possibility.  Prodigiosin is an aromatic compound that does not contain sulfur.
Interestingly, The ability of pigmented strains of Serratia marcescens to grow on bread has led to a possible explanation for transubstantiation miracles, in which eucharistic bread is converted into the body of Christ. Such miracles led to Pope Urban IV to institut the feast of Corpus Christi in 1264. This followed celebration of a mass of Bolsena in 1263, led by a Bohemian priest who had doubts concerning transsubstantiation.  During the Mass, the eucharist appeared to bleed, and each time the priest wiped away the blood, more would appear. This event is celebrated in a fresco in the Pontifical Palace in the Vatican City, painted by Raphael.

Proteobacteria

PmpA of Serratia sp.

 
9.B.102.5.3

Uncharacterized protein of 378  aas and 9 TMSs.  The N-terminal 4 TMSs match PmpA (TC# 9.B.102.5.2) while the C-terminal 4 TMSs match PmpB (TC# 9.B.102.5.5) as top hits.  Only the central TMS does not show homology.  Therefore, the N-terminus of this protein may have its N-terminus inside and its C-terminus outside.  Further, this provides evidence that PmpA and PmpB are two parts of a single two subunit transporter.  Prodigiosin, which is hypothesized to export prodigiosin in Serratia species, could be the function of this protein since Galdieria species are sensitive to prodigiosin.  Thus it could be a prodigiosin efflux pump (Lee et al. 2017). 

Red algae

UP of Galdieria sulphuraria

 
9.B.102.5.4

Uncharacterized protein of 353 as and 9 TMSs.  Similar to TC#9.B.102.5.3 (see the description of this protein).

red algae

UP of Galdieria sulphuraria

 
9.B.102.5.5

4 TMS protein of 142 aas, PmpB.  It has N- and C-termini predicted to be on the inside.  The opposite orientation is observed for PmpA (TC# 9.B.102.5.2) which in encoded by a gene adjacent to the pmpB gene.  These two proteins may comprise a single two subunit transporter.  These two genes are adjacent to pmpC which encodes a member of the TSUP family of sulfur compound uptake permeases (Gristwood et al., 2011, Shlykov et al., 2012).

Proteobacteria

PmpB of Serratia sp. (E7BBJ2)

 
9.B.102.5.6

YeeE homologue of 137 aas

Bacteroidetes

YeeE homologue of Psychroflexus torquis

 
9.B.102.5.7

YeeE homologue of 158 aas and 4 TMSs

Proteobacteria

YeeE homologue of Thiomonas intermedia (Thiobacillus intermedius)

 
9.B.102.5.8

YeeE homologue of 369 aas and 8 TMSs

Fungi

YeeE homologue of Rhodosporidium toruloides (Yeast) (Rhodotorula gracilis)

 
Examples:

TC#NameOrganismal TypeExample
Examples:

TC#NameOrganismal TypeExample
Examples:

TC#NameOrganismal TypeExample