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The Enterobacterium Trabulsiella odontotermitis Presents Novel Adaptations Related to Its Association with Fungus-Growing Termites.

Sapountzis P, Gruntjes T, Otani S, Estevez J, da Costa RR, Plunkett G, Perna NT, Poulsen M - Appl. Environ. Microbiol. (2015)

Bottom Line: Fungus-growing termites rely on symbiotic microorganisms to help break down plant material and to obtain nutrients.Taking diverse approaches, we obtained a solid phylogenetic placement of T. odontotermitis among the Enterobacteriaceae, investigated the physiology and enzymatic profiles of T. odontotermitis isolates, determined the localization of the bacterium in the termite gut, compared draft genomes of two T. odontotermitis isolates to those of their close relatives, and examined the expression of genes relevant to host colonization and putative symbiont functions.Our findings support the hypothesis that T. odontotermitis is a facultative symbiont mainly located in the paunch compartment of the gut, with possible roles in carbohydrate metabolism and aflatoxin degradation, while displaying adaptations to association with the termite host, such as expressing genes for a type VI secretion system which has been demonstrated to assist bacterial competition, colonization, and survival within hosts.

View Article: PubMed Central - PubMed

Affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark Sapountzis@bio.ku.dk.

No MeSH data available.


Schematic representations of the three different T6SS gene clusters in T. odontotermitis Mn101-3w2C (dark blue), T. odontotermitis Mn107-5a2c (light blue), and T. guamensis (brown). Arrows are proportional to the sizes (bp) of the genes in the three loci, and the orientations of genes are indicated. KEGG annotations of the predicted proteins are given below each arrow (ORF). Loci I and III have several genes with similarities in the amino acid sequences of their predicted proteins (E values of >1e−50; similarities of >50%). All paralogs are highlighted and connected with gray shading. The gray asterisks show paralogs that exist in T. odontotermitis but not in T. guamensis. For more details regarding all T6SS loci in all three Trabulsiella strains, see Table S5 in the supplemental material. Colored bars under the genes (arrows) show the gene expression results for M. natalensis (Mn) and Odontotermes sp. (Od) worker guts (red, no expression; green or blue, expression of the gene). A bar placed under the middle of a gene means that the primers used were specific only for that gene; a bar placed between two neighboring genes means that the primers were specific for two different neighboring genes and therefore amplified part of each gene and the region between them (in order to investigate whether they are expressed as an operon).
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Figure 4: Schematic representations of the three different T6SS gene clusters in T. odontotermitis Mn101-3w2C (dark blue), T. odontotermitis Mn107-5a2c (light blue), and T. guamensis (brown). Arrows are proportional to the sizes (bp) of the genes in the three loci, and the orientations of genes are indicated. KEGG annotations of the predicted proteins are given below each arrow (ORF). Loci I and III have several genes with similarities in the amino acid sequences of their predicted proteins (E values of >1e−50; similarities of >50%). All paralogs are highlighted and connected with gray shading. The gray asterisks show paralogs that exist in T. odontotermitis but not in T. guamensis. For more details regarding all T6SS loci in all three Trabulsiella strains, see Table S5 in the supplemental material. Colored bars under the genes (arrows) show the gene expression results for M. natalensis (Mn) and Odontotermes sp. (Od) worker guts (red, no expression; green or blue, expression of the gene). A bar placed under the middle of a gene means that the primers used were specific only for that gene; a bar placed between two neighboring genes means that the primers were specific for two different neighboring genes and therefore amplified part of each gene and the region between them (in order to investigate whether they are expressed as an operon).

Mentions: A striking difference between the two T. odontotermitis isolates and other Enterobacteriaceae (including T. guamensis) was the absence of type II, type III, and type IV secretion systems in T. odontotermitis. However, all three Trabulsiella strains have type VI secretion system (T6SS) genes on three different loci, similar to Erwinia sp., Pantoea sp., and Pseudomonas aeruginosa (36, 37). Two of the three loci appear to be conserved in Trabulsiella, while one differs between T. odontotermitis and T. guamensis (Fig. 4; see Table S5 in the supplemental material). Based on amino acid comparisons, all locus II and almost half of the locus III components (11/23 components) are more similar to T6SS components in Yersinia sp., while approximately half of the components of locus I (10/20 components in Mn101-3w2C and 13/20 components in Mn107-5a2c) are more similar to components in S. enterica, where they have been hypothesized to be essential for survival in and colonization of host cells (38). Expression analysis using Trabulsiella T6SS-specific primers showed that T6SS genes from all three loci are transcribed in Odontotermes species and from two out of three loci in M. natalensis (Fig. 4; see Fig. S1). More specifically, the three copies of icmF are transcribed from their respective loci, impC is expressed from both loci checked, and impJ/vasE is expressed from its single locus, while RT-PCR did not reveal detectable transcription for the vasG/clpV genes at both loci examined (Fig. 4).


The Enterobacterium Trabulsiella odontotermitis Presents Novel Adaptations Related to Its Association with Fungus-Growing Termites.

Sapountzis P, Gruntjes T, Otani S, Estevez J, da Costa RR, Plunkett G, Perna NT, Poulsen M - Appl. Environ. Microbiol. (2015)

Schematic representations of the three different T6SS gene clusters in T. odontotermitis Mn101-3w2C (dark blue), T. odontotermitis Mn107-5a2c (light blue), and T. guamensis (brown). Arrows are proportional to the sizes (bp) of the genes in the three loci, and the orientations of genes are indicated. KEGG annotations of the predicted proteins are given below each arrow (ORF). Loci I and III have several genes with similarities in the amino acid sequences of their predicted proteins (E values of >1e−50; similarities of >50%). All paralogs are highlighted and connected with gray shading. The gray asterisks show paralogs that exist in T. odontotermitis but not in T. guamensis. For more details regarding all T6SS loci in all three Trabulsiella strains, see Table S5 in the supplemental material. Colored bars under the genes (arrows) show the gene expression results for M. natalensis (Mn) and Odontotermes sp. (Od) worker guts (red, no expression; green or blue, expression of the gene). A bar placed under the middle of a gene means that the primers used were specific only for that gene; a bar placed between two neighboring genes means that the primers were specific for two different neighboring genes and therefore amplified part of each gene and the region between them (in order to investigate whether they are expressed as an operon).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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Figure 4: Schematic representations of the three different T6SS gene clusters in T. odontotermitis Mn101-3w2C (dark blue), T. odontotermitis Mn107-5a2c (light blue), and T. guamensis (brown). Arrows are proportional to the sizes (bp) of the genes in the three loci, and the orientations of genes are indicated. KEGG annotations of the predicted proteins are given below each arrow (ORF). Loci I and III have several genes with similarities in the amino acid sequences of their predicted proteins (E values of >1e−50; similarities of >50%). All paralogs are highlighted and connected with gray shading. The gray asterisks show paralogs that exist in T. odontotermitis but not in T. guamensis. For more details regarding all T6SS loci in all three Trabulsiella strains, see Table S5 in the supplemental material. Colored bars under the genes (arrows) show the gene expression results for M. natalensis (Mn) and Odontotermes sp. (Od) worker guts (red, no expression; green or blue, expression of the gene). A bar placed under the middle of a gene means that the primers used were specific only for that gene; a bar placed between two neighboring genes means that the primers were specific for two different neighboring genes and therefore amplified part of each gene and the region between them (in order to investigate whether they are expressed as an operon).
Mentions: A striking difference between the two T. odontotermitis isolates and other Enterobacteriaceae (including T. guamensis) was the absence of type II, type III, and type IV secretion systems in T. odontotermitis. However, all three Trabulsiella strains have type VI secretion system (T6SS) genes on three different loci, similar to Erwinia sp., Pantoea sp., and Pseudomonas aeruginosa (36, 37). Two of the three loci appear to be conserved in Trabulsiella, while one differs between T. odontotermitis and T. guamensis (Fig. 4; see Table S5 in the supplemental material). Based on amino acid comparisons, all locus II and almost half of the locus III components (11/23 components) are more similar to T6SS components in Yersinia sp., while approximately half of the components of locus I (10/20 components in Mn101-3w2C and 13/20 components in Mn107-5a2c) are more similar to components in S. enterica, where they have been hypothesized to be essential for survival in and colonization of host cells (38). Expression analysis using Trabulsiella T6SS-specific primers showed that T6SS genes from all three loci are transcribed in Odontotermes species and from two out of three loci in M. natalensis (Fig. 4; see Fig. S1). More specifically, the three copies of icmF are transcribed from their respective loci, impC is expressed from both loci checked, and impJ/vasE is expressed from its single locus, while RT-PCR did not reveal detectable transcription for the vasG/clpV genes at both loci examined (Fig. 4).

Bottom Line: Fungus-growing termites rely on symbiotic microorganisms to help break down plant material and to obtain nutrients.Taking diverse approaches, we obtained a solid phylogenetic placement of T. odontotermitis among the Enterobacteriaceae, investigated the physiology and enzymatic profiles of T. odontotermitis isolates, determined the localization of the bacterium in the termite gut, compared draft genomes of two T. odontotermitis isolates to those of their close relatives, and examined the expression of genes relevant to host colonization and putative symbiont functions.Our findings support the hypothesis that T. odontotermitis is a facultative symbiont mainly located in the paunch compartment of the gut, with possible roles in carbohydrate metabolism and aflatoxin degradation, while displaying adaptations to association with the termite host, such as expressing genes for a type VI secretion system which has been demonstrated to assist bacterial competition, colonization, and survival within hosts.

View Article: PubMed Central - PubMed

Affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark Sapountzis@bio.ku.dk.

No MeSH data available.