Bacterial phylogeny structures soil resistomes across habitats

By Kevin J. Forsberg, Sanket Patel, Molly K. Gibson, C. Lauber, Rob Knight, Noah Fierer, Gautam Dantas. Nature, 2014

1,084 citations recorded by the source corpus.

Ancient and diverse antibiotic resistance genes (ARGs) have previously been identified from soil, including genes identical to those in human pathogens. Despite the apparent overlap between soil and clinical resistomes, factors influencing ARG composition in soil and their movement between genomes and habitats remain largely unknown. General metagenome functions often correlate with the underlying structure of bacterial communities. However, ARGs are proposed to be highly mobile, prompting speculation that resistomes may not correlate with phylogenetic signatures or ecological divisions. To investigate these relationships, we performed functional metagenomic selections for resistance to 18 antibiotics from 18 agricultural and grassland soils. The 2,895 ARGs we discovered were mostly new, and represent all major resistance mechanisms. We demonstrate that distinct soil types harbour distinct resistomes, and that the addition of nitrogen fertilizer strongly influenced soil ARG content. Resistome composition also correlated with microbial phylogenetic and taxonomic structure, both across and within soil types. Consistent with this strong correlation, mobility elements (genes responsible for horizontal gene transfer between bacteria such as transposases and integrases) syntenic with ARGs were rare in soil by comparison with sequenced pathogens, suggesting that ARGs may not transfer between soil bacteria as readily as is observed between human pathogens. Together, our results indicate that bacterial community composition is the primary determinant of soil ARG content, challenging previous hypotheses that horizontal gene transfer effectively decouples resistomes from phylogeny.

Subfields: Clinical Biochemistry, Genetics, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/ed582e27cfd9fa8cc99b447273ce3464838b78b3

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Clinical Biochemistry

1. James M. Tiedje
2. Konstantinos T. Konstantinidis
3. L. Rodriguez-R.
4. Marc Ereshefsky
5. Kateryna Selezska

In Genetics

1. James M. Tiedje
2. Yong-guan Zhu

In Molecular Biology

1. Yong-guan Zhu
2. Tong Zhang
3. Gautam Dantas
4. Molly K. Gibson
5. Xinli An
6. James M. Tiedje
7. B. Aslam
8. Hu Li

Citations in the corpus

• Antibiotic resistance: a rundown of a global crisis (2018, background): “For that reason, antibiotic resistance may simply depict the Darwinian competition from natural microbial-derived antimicrobial elements.(29,30) The functional meta-genomic analysis of soil microbes has revealed an extensive diversity in genetic determinants associated with antibiotic resistance.”
• Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology (2014, result): “The low ratio of class C b-lactamases to class B b-lactamases in the soil supports previous findings in studies of the soil resistome (Allen et al., 2008; Forsberg et al., 2014); however, our results indicate that this trend is opposite in the human gut resistome (class C/class B ratio: 0.”
• Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes (2015, background): “Previous study indicated that ARG composition correlated with microbial phylogenetic and taxonomic structure both across and within soil types, that is, bacterial community composition was the primary determinant of soil ARG contents (Forsberg et al., 2014); therefore, the co-occurrence patterns bet”
• Comparison on the structure and function of the rhizosphere microbial community between healthy and root-rot Panax notoginseng (2016, background): “PICRUSt has allowed deeper insights into thousands of uncultivated microbial communities for which only marker gene surveys are currently available (Forsberg et al., 2014).”
• Do manure-borne or indigenous soil microorganisms influence the spread of antibiotic resistance genes in manured soil? (2017, background): “Based on the non-random co-occurrence between ARGs and bacterial taxa, this approach might represent an appropriate strategy to track potential ARG hosts (Forsberg et al., 2014; Li et al., 2015).”