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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

Heat map representing relative expression levels of resistance genes in the gut microbiota of individual humans, pigs and mice.Resistance genes are grouped based on resistance against ten types of antibiotics.
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f3: Heat map representing relative expression levels of resistance genes in the gut microbiota of individual humans, pigs and mice.Resistance genes are grouped based on resistance against ten types of antibiotics.

Mentions: The distribution of reads aligning to resistance genes that confer resistance against ten different types of antibiotics was analysed. Genes in the RED-DB are grouped according to resistance against the following types of antibiotics: aminoglycosides, β-lactams, chloramphenicol, glycopeptides, macrolides, oxazolidinones, quinolones, sulphonamides, tetracyclines and trimethoprim. Expression of genes involved in resistance against most types of antibiotics (6/10) was detected at least in one of the datasets analysed, with the exception of genes conferring resistance against quinolone, oxazolidinone, sulphonamide and trimethoprim antibiotics (Fig. 2). In human gut microbiota β-lactam, aminoglycoside, macrolide and tetracycline resistance genes were expressed. In mice intestinal content samples, in which the cumulative relative expression of resistance genes was the lowest for all gut-associated niches examined here, primarily tetracycline resistance genes were found to be expressed. One-way ANOSIM showed that resistance profiles were not significantly different between different mammalian hosts when comparing the groups of human adults, mice and pigs (global R = 0,089 p = 0.197). A comparison of antibiotic resistance gene expression profiles of the microbiota of individual human adults, pigs and mice indicated there are substantial inter-individual differences within the groups (Fig. 3). In the intestinal samples obtained from the human infant, only the expression of a tetracycline resistance gene was detected. The profiles of expressed resistance genes observed in forest soil and sub-seafloor sediment communities stood out because expression of chloramphenicol resistance genes made up ≥20% of the cumulative total whereas in the other ecological niches they were not detected. In sea bacterioplankton and the marine sponge the expression of two β-lactam resistance genes was detected, namely blaTEM-1 and blaTEM-116. These genes share 97% nucleotide identity and therefore it is possible that in reality only a single β-lactam resistance gene is being expressed that is closely related to the two known genes. In sea bacterioplankton as much as 0.7% of the non-ribosomal transcripts aligned with the two blaTEM genes.


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)

Heat map representing relative expression levels of resistance genes in the gut microbiota of individual humans, pigs and mice.Resistance genes are grouped based on resistance against ten types of antibiotics.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Heat map representing relative expression levels of resistance genes in the gut microbiota of individual humans, pigs and mice.Resistance genes are grouped based on resistance against ten types of antibiotics.
Mentions: The distribution of reads aligning to resistance genes that confer resistance against ten different types of antibiotics was analysed. Genes in the RED-DB are grouped according to resistance against the following types of antibiotics: aminoglycosides, β-lactams, chloramphenicol, glycopeptides, macrolides, oxazolidinones, quinolones, sulphonamides, tetracyclines and trimethoprim. Expression of genes involved in resistance against most types of antibiotics (6/10) was detected at least in one of the datasets analysed, with the exception of genes conferring resistance against quinolone, oxazolidinone, sulphonamide and trimethoprim antibiotics (Fig. 2). In human gut microbiota β-lactam, aminoglycoside, macrolide and tetracycline resistance genes were expressed. In mice intestinal content samples, in which the cumulative relative expression of resistance genes was the lowest for all gut-associated niches examined here, primarily tetracycline resistance genes were found to be expressed. One-way ANOSIM showed that resistance profiles were not significantly different between different mammalian hosts when comparing the groups of human adults, mice and pigs (global R = 0,089 p = 0.197). A comparison of antibiotic resistance gene expression profiles of the microbiota of individual human adults, pigs and mice indicated there are substantial inter-individual differences within the groups (Fig. 3). In the intestinal samples obtained from the human infant, only the expression of a tetracycline resistance gene was detected. The profiles of expressed resistance genes observed in forest soil and sub-seafloor sediment communities stood out because expression of chloramphenicol resistance genes made up ≥20% of the cumulative total whereas in the other ecological niches they were not detected. In sea bacterioplankton and the marine sponge the expression of two β-lactam resistance genes was detected, namely blaTEM-1 and blaTEM-116. These genes share 97% nucleotide identity and therefore it is possible that in reality only a single β-lactam resistance gene is being expressed that is closely related to the two known genes. In sea bacterioplankton as much as 0.7% of the non-ribosomal transcripts aligned with the two blaTEM genes.

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