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Mining microbial metatranscriptomes for expression of antibiotic resistance genes under natural conditions.

Versluis D, D'Andrea MM, Ramiro Garcia J, Leimena MM, Hugenholtz F, Zhang J, Öztürk B, Nylund L, Sipkema D, van Schaik W, de Vos WM, Kleerebezem M, Smidt H, van Passel MW - Sci Rep (2015)

Bottom Line: We found that resistance genes are expressed in all studied ecological niches, albeit with niche-specific differences in relative expression levels and diversity of transcripts.Resistance gene expression could result from the presence of natural antibiotics in the environment, although we could not link it to expression of corresponding secondary metabolites biosynthesis clusters.Alternatively, resistance gene expression could be constitutive, or these genes serve alternative roles besides antibiotic resistance.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands.

ABSTRACT
Antibiotic resistance genes are found in a broad range of ecological niches associated with complex microbiota. Here we investigated if resistance genes are not only present, but also transcribed under natural conditions. Furthermore, we examined the potential for antibiotic production by assessing the expression of associated secondary metabolite biosynthesis gene clusters. Metatranscriptome datasets from intestinal microbiota of four human adults, one human infant, 15 mice and six pigs, of which only the latter have received antibiotics prior to the study, as well as from sea bacterioplankton, a marine sponge, forest soil and sub-seafloor sediment, were investigated. We found that resistance genes are expressed in all studied ecological niches, albeit with niche-specific differences in relative expression levels and diversity of transcripts. For example, in mice and human infant microbiota predominantly tetracycline resistance genes were expressed while in human adult microbiota the spectrum of expressed genes was more diverse, and also included β-lactam, aminoglycoside and macrolide resistance genes. Resistance gene expression could result from the presence of natural antibiotics in the environment, although we could not link it to expression of corresponding secondary metabolites biosynthesis clusters. Alternatively, resistance gene expression could be constitutive, or these genes serve alternative roles besides antibiotic resistance.

No MeSH data available.


Related in: MedlinePlus

Cumulative relative expression of secondary metabolite biosynthesis domains involved in the production of type I polyketides, type II polyketides, non-ribosomal peptides and aminoglycosides.Error bars represent one standard deviation.
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f5: Cumulative relative expression of secondary metabolite biosynthesis domains involved in the production of type I polyketides, type II polyketides, non-ribosomal peptides and aminoglycosides.Error bars represent one standard deviation.

Mentions: We also investigated whether the expression of antibiotic resistance genes can be associated with local antibiotic biosynthesis. To this end, we used the antibiotics and secondary metabolite analysis shell (antiSMASH) pipeline, which focuses on the production of secondary metabolites, amongst which are also antibiotics20. Profile hidden Markov Models (hMMs) from antiSMASH of domains of enzymes involved in the construction of the backbones of various types of antibiotics were used to investigate antibiotic biosynthesis. We investigated genes responsible for the biosynthesis of type I and II polyketides, non-ribosomal peptides and aminoglycosides/aminocyclitols (see Supplementary Table S3 for the domains and the complete results), which can be involved in, respectively, the biosynthesis of macrolides, tetracyclines, β-lactams and aminoglycosides (Fig. 5). In the gut microbiota of humans (adult and infant), pigs and mice, the marine sponge and sub-seafloor sediment, very little expression of SMB genes was detected. The lowest relative expression of SMB genes was found in human individual one, for whom only a single domain was detected by just five reads, suggesting that expression of SMB genes was very low. The expression of SMB genes in sea bacterioplankton and forest soil was at least an order of magnitude higher than in the other investigated environments. No associations between the expression of specific SMB clusters and resistance genes were uncovered, and their cumulative expression levels varied per ecological niche (Supplementary Fig. S2).


Mining microbial metatranscriptomes for expression of antibiotic resistance genes under natural conditions.

Versluis D, D'Andrea MM, Ramiro Garcia J, Leimena MM, Hugenholtz F, Zhang J, Öztürk B, Nylund L, Sipkema D, van Schaik W, de Vos WM, Kleerebezem M, Smidt H, van Passel MW - Sci Rep (2015)

Cumulative relative expression of secondary metabolite biosynthesis domains involved in the production of type I polyketides, type II polyketides, non-ribosomal peptides and aminoglycosides.Error bars represent one standard deviation.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4495384&req=5

f5: Cumulative relative expression of secondary metabolite biosynthesis domains involved in the production of type I polyketides, type II polyketides, non-ribosomal peptides and aminoglycosides.Error bars represent one standard deviation.
Mentions: We also investigated whether the expression of antibiotic resistance genes can be associated with local antibiotic biosynthesis. To this end, we used the antibiotics and secondary metabolite analysis shell (antiSMASH) pipeline, which focuses on the production of secondary metabolites, amongst which are also antibiotics20. Profile hidden Markov Models (hMMs) from antiSMASH of domains of enzymes involved in the construction of the backbones of various types of antibiotics were used to investigate antibiotic biosynthesis. We investigated genes responsible for the biosynthesis of type I and II polyketides, non-ribosomal peptides and aminoglycosides/aminocyclitols (see Supplementary Table S3 for the domains and the complete results), which can be involved in, respectively, the biosynthesis of macrolides, tetracyclines, β-lactams and aminoglycosides (Fig. 5). In the gut microbiota of humans (adult and infant), pigs and mice, the marine sponge and sub-seafloor sediment, very little expression of SMB genes was detected. The lowest relative expression of SMB genes was found in human individual one, for whom only a single domain was detected by just five reads, suggesting that expression of SMB genes was very low. The expression of SMB genes in sea bacterioplankton and forest soil was at least an order of magnitude higher than in the other investigated environments. No associations between the expression of specific SMB clusters and resistance genes were uncovered, and their cumulative expression levels varied per ecological niche (Supplementary Fig. S2).

Bottom Line: We found that resistance genes are expressed in all studied ecological niches, albeit with niche-specific differences in relative expression levels and diversity of transcripts.Resistance gene expression could result from the presence of natural antibiotics in the environment, although we could not link it to expression of corresponding secondary metabolites biosynthesis clusters.Alternatively, resistance gene expression could be constitutive, or these genes serve alternative roles besides antibiotic resistance.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands.

ABSTRACT
Antibiotic resistance genes are found in a broad range of ecological niches associated with complex microbiota. Here we investigated if resistance genes are not only present, but also transcribed under natural conditions. Furthermore, we examined the potential for antibiotic production by assessing the expression of associated secondary metabolite biosynthesis gene clusters. Metatranscriptome datasets from intestinal microbiota of four human adults, one human infant, 15 mice and six pigs, of which only the latter have received antibiotics prior to the study, as well as from sea bacterioplankton, a marine sponge, forest soil and sub-seafloor sediment, were investigated. We found that resistance genes are expressed in all studied ecological niches, albeit with niche-specific differences in relative expression levels and diversity of transcripts. For example, in mice and human infant microbiota predominantly tetracycline resistance genes were expressed while in human adult microbiota the spectrum of expressed genes was more diverse, and also included β-lactam, aminoglycoside and macrolide resistance genes. Resistance gene expression could result from the presence of natural antibiotics in the environment, although we could not link it to expression of corresponding secondary metabolites biosynthesis clusters. Alternatively, resistance gene expression could be constitutive, or these genes serve alternative roles besides antibiotic resistance.

No MeSH data available.


Related in: MedlinePlus