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Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria.

Salomon D, Klimko JA, Trudgian DC, Kinch LN, Grishin NV, Mirzaei H, Orth K - PLoS Pathog. (2015)

Bottom Line: Using comparative proteomics and genetics, we identified their effector repertoires.We also showed that the T6SS2 secretes at least three antibacterial effectors.We demonstrated that a MIX V-effector from V. alginolyticus is a functional T6SS effector when ectopically expressed in another Vibrio species.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, United States of America.

ABSTRACT
The type VI secretion system (T6SS) is a widespread protein secretion apparatus used by Gram-negative bacteria to deliver toxic effector proteins into adjacent bacterial or host cells. Here, we uncovered a role in interbacterial competition for the two T6SSs encoded by the marine pathogen Vibrio alginolyticus. Using comparative proteomics and genetics, we identified their effector repertoires. In addition to the previously described effector V12G01_02265, we identified three new effectors secreted by T6SS1, indicating that the T6SS1 secretes at least four antibacterial effectors, of which three are members of the MIX-effector class. We also showed that the T6SS2 secretes at least three antibacterial effectors. Our findings revealed that many MIX-effectors belonging to clan V are "orphan" effectors that neighbor mobile elements and are shared between marine bacteria via horizontal gene transfer. We demonstrated that a MIX V-effector from V. alginolyticus is a functional T6SS effector when ectopically expressed in another Vibrio species. We propose that mobile MIX V-effectors serve as an environmental reservoir of T6SS effectors that are shared and used to diversify antibacterial toxin repertoires in marine bacteria, resulting in enhanced competitive fitness.

No MeSH data available.


Related in: MedlinePlus

Mobility of MIX V-effector/immunity cassettes.Genome neighborhoods are illustrated using arrows to indicate gene orientation, with gene correspondence between species indicated by black vertical lines and omitted genes indicated in parentheses. (A) The “orphan” Duf2235-containing MIX V-effector/immunity pair (va02265/0, filled red arrows) encoded by the V. alginolyticus 12G01 scaffold (V.alg12G01) falls within a conserved gene neighborhood present in other V. alginolyticus strains (green arrows). The orphan pair is absent from the alternate V. alginolyticus strain genomes and is replaced by an alternate cassette of 3 different genes (open red arrows) in V. alginolyticus NBRC 15630 = ATCC 17749 chromosome 2 (V.algNBRC15630) and an unknown gene in V. alginolyticus 40B scaffold (V.alg40B). A homologous Duf2235-containing MIX V-effector with a duplicated immunity gene (filled red arrows) can be found in a more distant Vibrio strain: V. anguillarum NB10 chromosome 2 (V.angNB10) in an alternate gene neighborhood (orange arrows). (B) The Colicin DNase-containing MIX V-effector/immunity pair (vpa1263/vti2, filled red arrows) encoded by V. parahaemolyticus RIMD 2210633 chromosome 2 (V.para.RIMD2) belongs to a genetic island that includes a transposon and phage integrase (pink arrows). The island is not present in similar strains such as V. parahaemolyticus BB22OP chromosome 2 (V.para.BB22OP) that retains the surrounding conserved gene neighborhood (purple arrows). A homologous Colicin DNase-containing MIX V-effector/immunity cassette (filled red arrows) is present in a more distant Vibrio strain, Vibrio campbellii ATCC BAA-1116 (V.campATCC), in an alternate gene neighborhood (cyan arrows). Neighborhoods include genes (from left to right): N646_ 3835—N646_3824 from V.alg.NBRC15630, V12G01_02235—V12G01_02286 and alternate genes V12G01_08143—V12G01_08023 from V.alg.12G01, VMC_26590—VMC_26680 for V.alg40B, VANGNB10_cII03835—VANGNB10_cII03824 for V.angNB10, VPBB_A1148—VPBB_A1154 for V.para.BB22OP, VPA1250—VPA1273 and alternate genes VP0094—VP0077 from V.para.RIMD, and VIBHAR_00561—VIBHAR_00534 from V.campATCC. Tspn = transposase, Int = integrase, Imm = immunity, Unk = unknown.
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ppat.1005128.g004: Mobility of MIX V-effector/immunity cassettes.Genome neighborhoods are illustrated using arrows to indicate gene orientation, with gene correspondence between species indicated by black vertical lines and omitted genes indicated in parentheses. (A) The “orphan” Duf2235-containing MIX V-effector/immunity pair (va02265/0, filled red arrows) encoded by the V. alginolyticus 12G01 scaffold (V.alg12G01) falls within a conserved gene neighborhood present in other V. alginolyticus strains (green arrows). The orphan pair is absent from the alternate V. alginolyticus strain genomes and is replaced by an alternate cassette of 3 different genes (open red arrows) in V. alginolyticus NBRC 15630 = ATCC 17749 chromosome 2 (V.algNBRC15630) and an unknown gene in V. alginolyticus 40B scaffold (V.alg40B). A homologous Duf2235-containing MIX V-effector with a duplicated immunity gene (filled red arrows) can be found in a more distant Vibrio strain: V. anguillarum NB10 chromosome 2 (V.angNB10) in an alternate gene neighborhood (orange arrows). (B) The Colicin DNase-containing MIX V-effector/immunity pair (vpa1263/vti2, filled red arrows) encoded by V. parahaemolyticus RIMD 2210633 chromosome 2 (V.para.RIMD2) belongs to a genetic island that includes a transposon and phage integrase (pink arrows). The island is not present in similar strains such as V. parahaemolyticus BB22OP chromosome 2 (V.para.BB22OP) that retains the surrounding conserved gene neighborhood (purple arrows). A homologous Colicin DNase-containing MIX V-effector/immunity cassette (filled red arrows) is present in a more distant Vibrio strain, Vibrio campbellii ATCC BAA-1116 (V.campATCC), in an alternate gene neighborhood (cyan arrows). Neighborhoods include genes (from left to right): N646_ 3835—N646_3824 from V.alg.NBRC15630, V12G01_02235—V12G01_02286 and alternate genes V12G01_08143—V12G01_08023 from V.alg.12G01, VMC_26590—VMC_26680 for V.alg40B, VANGNB10_cII03835—VANGNB10_cII03824 for V.angNB10, VPBB_A1148—VPBB_A1154 for V.para.BB22OP, VPA1250—VPA1273 and alternate genes VP0094—VP0077 from V.para.RIMD, and VIBHAR_00561—VIBHAR_00534 from V.campATCC. Tspn = transposase, Int = integrase, Imm = immunity, Unk = unknown.

Mentions: We next examined whether the VaT6SS1 effector/immunity pairs that we identified in the 12G01 strain were also found in other V. alginolyticus strains. Homologs of the effector Va01435, as well as of the two MIX-effectors Va01565 and Va16152, and their cognate immunity proteins were encoded in the genomes of other sequenced V. alginolyticus strains (i.e. NBRC 15630, E0666, and 40B) in the same synteny as in strain 12G01. However, the bicistronic unit encoding the MIX-effector/immunity pair Va02265/0 was not found in the genomes of other sequenced V. alginolyticus strains (Fig 4A), suggesting that it was recently acquired by the 12G01 strain. Interestingly, we found bicistronic units encoding homologs of the Va02265/0 MIX-effector/immunity cassette in genomes of other Vibrio species (e.g. V. anguillarum NB10), albeit at a synteny distinct from the one it had in V. alginolyticus 12G01 (Fig 4A). These results suggested that this MIX-effector/immunity cassette might be transmitted horizontally between Vibrio species.


Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria.

Salomon D, Klimko JA, Trudgian DC, Kinch LN, Grishin NV, Mirzaei H, Orth K - PLoS Pathog. (2015)

Mobility of MIX V-effector/immunity cassettes.Genome neighborhoods are illustrated using arrows to indicate gene orientation, with gene correspondence between species indicated by black vertical lines and omitted genes indicated in parentheses. (A) The “orphan” Duf2235-containing MIX V-effector/immunity pair (va02265/0, filled red arrows) encoded by the V. alginolyticus 12G01 scaffold (V.alg12G01) falls within a conserved gene neighborhood present in other V. alginolyticus strains (green arrows). The orphan pair is absent from the alternate V. alginolyticus strain genomes and is replaced by an alternate cassette of 3 different genes (open red arrows) in V. alginolyticus NBRC 15630 = ATCC 17749 chromosome 2 (V.algNBRC15630) and an unknown gene in V. alginolyticus 40B scaffold (V.alg40B). A homologous Duf2235-containing MIX V-effector with a duplicated immunity gene (filled red arrows) can be found in a more distant Vibrio strain: V. anguillarum NB10 chromosome 2 (V.angNB10) in an alternate gene neighborhood (orange arrows). (B) The Colicin DNase-containing MIX V-effector/immunity pair (vpa1263/vti2, filled red arrows) encoded by V. parahaemolyticus RIMD 2210633 chromosome 2 (V.para.RIMD2) belongs to a genetic island that includes a transposon and phage integrase (pink arrows). The island is not present in similar strains such as V. parahaemolyticus BB22OP chromosome 2 (V.para.BB22OP) that retains the surrounding conserved gene neighborhood (purple arrows). A homologous Colicin DNase-containing MIX V-effector/immunity cassette (filled red arrows) is present in a more distant Vibrio strain, Vibrio campbellii ATCC BAA-1116 (V.campATCC), in an alternate gene neighborhood (cyan arrows). Neighborhoods include genes (from left to right): N646_ 3835—N646_3824 from V.alg.NBRC15630, V12G01_02235—V12G01_02286 and alternate genes V12G01_08143—V12G01_08023 from V.alg.12G01, VMC_26590—VMC_26680 for V.alg40B, VANGNB10_cII03835—VANGNB10_cII03824 for V.angNB10, VPBB_A1148—VPBB_A1154 for V.para.BB22OP, VPA1250—VPA1273 and alternate genes VP0094—VP0077 from V.para.RIMD, and VIBHAR_00561—VIBHAR_00534 from V.campATCC. Tspn = transposase, Int = integrase, Imm = immunity, Unk = unknown.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4549250&req=5

ppat.1005128.g004: Mobility of MIX V-effector/immunity cassettes.Genome neighborhoods are illustrated using arrows to indicate gene orientation, with gene correspondence between species indicated by black vertical lines and omitted genes indicated in parentheses. (A) The “orphan” Duf2235-containing MIX V-effector/immunity pair (va02265/0, filled red arrows) encoded by the V. alginolyticus 12G01 scaffold (V.alg12G01) falls within a conserved gene neighborhood present in other V. alginolyticus strains (green arrows). The orphan pair is absent from the alternate V. alginolyticus strain genomes and is replaced by an alternate cassette of 3 different genes (open red arrows) in V. alginolyticus NBRC 15630 = ATCC 17749 chromosome 2 (V.algNBRC15630) and an unknown gene in V. alginolyticus 40B scaffold (V.alg40B). A homologous Duf2235-containing MIX V-effector with a duplicated immunity gene (filled red arrows) can be found in a more distant Vibrio strain: V. anguillarum NB10 chromosome 2 (V.angNB10) in an alternate gene neighborhood (orange arrows). (B) The Colicin DNase-containing MIX V-effector/immunity pair (vpa1263/vti2, filled red arrows) encoded by V. parahaemolyticus RIMD 2210633 chromosome 2 (V.para.RIMD2) belongs to a genetic island that includes a transposon and phage integrase (pink arrows). The island is not present in similar strains such as V. parahaemolyticus BB22OP chromosome 2 (V.para.BB22OP) that retains the surrounding conserved gene neighborhood (purple arrows). A homologous Colicin DNase-containing MIX V-effector/immunity cassette (filled red arrows) is present in a more distant Vibrio strain, Vibrio campbellii ATCC BAA-1116 (V.campATCC), in an alternate gene neighborhood (cyan arrows). Neighborhoods include genes (from left to right): N646_ 3835—N646_3824 from V.alg.NBRC15630, V12G01_02235—V12G01_02286 and alternate genes V12G01_08143—V12G01_08023 from V.alg.12G01, VMC_26590—VMC_26680 for V.alg40B, VANGNB10_cII03835—VANGNB10_cII03824 for V.angNB10, VPBB_A1148—VPBB_A1154 for V.para.BB22OP, VPA1250—VPA1273 and alternate genes VP0094—VP0077 from V.para.RIMD, and VIBHAR_00561—VIBHAR_00534 from V.campATCC. Tspn = transposase, Int = integrase, Imm = immunity, Unk = unknown.
Mentions: We next examined whether the VaT6SS1 effector/immunity pairs that we identified in the 12G01 strain were also found in other V. alginolyticus strains. Homologs of the effector Va01435, as well as of the two MIX-effectors Va01565 and Va16152, and their cognate immunity proteins were encoded in the genomes of other sequenced V. alginolyticus strains (i.e. NBRC 15630, E0666, and 40B) in the same synteny as in strain 12G01. However, the bicistronic unit encoding the MIX-effector/immunity pair Va02265/0 was not found in the genomes of other sequenced V. alginolyticus strains (Fig 4A), suggesting that it was recently acquired by the 12G01 strain. Interestingly, we found bicistronic units encoding homologs of the Va02265/0 MIX-effector/immunity cassette in genomes of other Vibrio species (e.g. V. anguillarum NB10), albeit at a synteny distinct from the one it had in V. alginolyticus 12G01 (Fig 4A). These results suggested that this MIX-effector/immunity cassette might be transmitted horizontally between Vibrio species.

Bottom Line: Using comparative proteomics and genetics, we identified their effector repertoires.We also showed that the T6SS2 secretes at least three antibacterial effectors.We demonstrated that a MIX V-effector from V. alginolyticus is a functional T6SS effector when ectopically expressed in another Vibrio species.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, United States of America.

ABSTRACT
The type VI secretion system (T6SS) is a widespread protein secretion apparatus used by Gram-negative bacteria to deliver toxic effector proteins into adjacent bacterial or host cells. Here, we uncovered a role in interbacterial competition for the two T6SSs encoded by the marine pathogen Vibrio alginolyticus. Using comparative proteomics and genetics, we identified their effector repertoires. In addition to the previously described effector V12G01_02265, we identified three new effectors secreted by T6SS1, indicating that the T6SS1 secretes at least four antibacterial effectors, of which three are members of the MIX-effector class. We also showed that the T6SS2 secretes at least three antibacterial effectors. Our findings revealed that many MIX-effectors belonging to clan V are "orphan" effectors that neighbor mobile elements and are shared between marine bacteria via horizontal gene transfer. We demonstrated that a MIX V-effector from V. alginolyticus is a functional T6SS effector when ectopically expressed in another Vibrio species. We propose that mobile MIX V-effectors serve as an environmental reservoir of T6SS effectors that are shared and used to diversify antibacterial toxin repertoires in marine bacteria, resulting in enhanced competitive fitness.

No MeSH data available.


Related in: MedlinePlus