A comprehensive survey of integron-associated genes present in metagenomes
Journal article, 2020

Background: Integrons are genomic elements that mediate horizontal gene transfer by inserting and removing genetic material using site-specific recombination. Integrons are commonly found in bacterial genomes, where they maintain a large and diverse set of genes that plays an important role in adaptation and evolution. Previous studies have started to characterize the wide range of biological functions present in integrons. However, the efforts have so far mainly been limited to genomes from cultivable bacteria and amplicons generated by PCR, thus targeting only a small part of the total integron diversity. Metagenomic data, generated by direct sequencing of environmental and clinical samples, provides a more holistic and unbiased analysis of integron-associated genes. However, the fragmented nature of metagenomic data has previously made such analysis highly challenging. Results: Here, we present a systematic survey of integron-associated genes in metagenomic data. The analysis was based on a newly developed computational method where integron-associated genes were identified by detecting their associated recombination sites. By processing contiguous sequences assembled from more than 10 terabases of metagenomic data, we were able to identify 13,397 unique integron-associated genes. Metagenomes from marine microbial communities had the highest occurrence of integron-associated genes with levels more than 100-fold higher than in the human microbiome. The identified genes had a large functional diversity spanning over several functional classes. Genes associated with defense mechanisms and mobility facilitators were most overrepresented and more than five times as common in integrons compared to other bacterial genes. As many as two thirds of the genes were found to encode proteins of unknown function. Less than 1% of the genes were associated with antibiotic resistance, of which several were novel, previously undescribed, resistance gene variants. Conclusions: Our results highlight the large functional diversity maintained by integrons present in unculturable bacteria and significantly expands the number of described integron-associated genes.

ORFans

Integrons

Metagenomics

Gene cassettes

Antibiotic resistance

Horizontal gene transfer

Functional annotation

Author

Mariana Buongermino Pereira

Chalmers, Mathematical Sciences, Applied Mathematics and Statistics

University of Gothenburg

Tobias Österlund

University of Gothenburg

Chalmers, Mathematical Sciences, Applied Mathematics and Statistics

Martin Eriksson

University of Gothenburg

Chalmers, Gothenburg Centre for Sustainable Development (GMV)

Thomas Backhaus

University of Gothenburg

Marina Axelson-Fisk

Chalmers, Mathematical Sciences, Applied Mathematics and Statistics

Erik Kristiansson

Chalmers, Mathematical Sciences, Applied Mathematics and Statistics

University of Gothenburg

BMC Genomics

1471-2164 (ISSN)

Vol. 21 1 495

Subject Categories

Microbiology

Bioinformatics and Systems Biology

Genetics

DOI

10.1186/s12864-020-06830-5

PubMed

32689930

More information

Latest update

9/1/2020 1