Novel and diverse integron integrase genes and integron‐like gene cassettes are prevalent in deep‐sea hydrothermal vents

Abstract

The lack of information about mobile DNA in deep-sea hydrothermal vents limits our understanding of the phylogenetic diversity of the mobile genome of bacteria in these environments. We used culture-independent techniques to explore the diversity of the integron/mobile gene cassette system in a variety of hydrothermal vent communities. Three samples, which included two different hydrothermal vent fluids and a mussel species that contained essentially monophyletic sulfur-oxidizing bacterial endosymbionts, were collected from Suiyo Seamount, Izu-Bonin, Japan, and Pika site, Mariana arc. First, using degenerate polymerase chain reaction (PCR) primers, we amplified integron integrase genes from metagenomic DNA from each sample. From vent fluids, we discovered 74 new integrase genes that were classified into 11 previously undescribed integron classes. One integrase gene was recorded in the mussel symbiont and was phylogenetically distant from those recovered from vent fluids. Second, using PCR primers targeting the gene cassette recombination site (59-be), we amplified and subsequently identified 60 diverse gene cassettes. In multicassette amplicons, a total of 13 59-be sites were identified. Most of these sites displayed features that were atypical of the features previously well conserved in this family. The Suiyo vent fluid was characterized by gene cassette open reading frames (ORFs) that had significant homologies with transferases, DNA-binding proteins and metal transporter proteins, while the majority of Pika vent fluid gene cassettes contained novel ORFs with no identifiable homologues in databases. The symbiont gene cassette ORFs were found to be matched with DNA repair proteins, methionine aminopeptidase, aminopeptidase N, O-sialoglycoprotein endopeptidase and glutamate synthase, which are proteins expected to play a role in animal/symbiont metabolism. The success of this study indicates that the integron/gene cassette system is common in deep-sea hydrothermal vents, an environment type well removed from anthropogenic disturbance.

Integrons: Past, Present, and Future

“…On the basis of carrying an IntI gene (intI), more than 15% of genome-sequenced bacteria appear to contain an integron (1,2). Integrons are also found in a wide diversity of environments, including forest soils, desert soils, riverine sediment, Antarctic soils, hot springs, aquatic biofilms, plant surfaces, marine sediment, and deep-sea sediment (15)(16)(17)(18)(19)(20).…”

The Integron: Adaptation On Demand

“…Integron cassettes seem ubiquitous-they have been recovered from every environment investigated, including soil, riverine sediment, seawater, biofilms, plant surfaces and even eukaryotes' symbionts (36,(75)(76)(77)(78)(79)(80)(81).…”

Inadequately Treated Wastewater as a Source of Human Enteric Viruses in the Environment

“…Among them, integrons are suspected to be the most important (Stalder et al 2012), since they are often associated with other mobile genetic elements, such as plasmids or transposons, and are detected in various environments and matrices (Rosser and Young 1999;Goldstein et al 2001;Elsaied et al 2007Elsaied et al , 2011Gillings et al 2009;Xia et al 2013). Integrons are widely distributed in gramnegative bacteria; however, recent studies indicate their presence also in gram-positive species (Xu et al 2001(Xu et al , 2010.…”

“…The spread of antimicrobial-resistance genes by integrons was extensively investigated primarily in clinical settings (Grape et al 2003;Pan et al 2006;Dubois et al 2007). Nowadays, increased interest in their environmental role is observed (Elsaied et al 2007;Gillings et al 2009;Elsaied et al 2011) and also reviewed by Stalder et al (2012). Integrons consist of integrase (intI) gene, a recombination site (attI) and one or two promoters (Recchia and Hall 1995).…”

“…Gene cassettes associated to class 1-3 integrons often confer resistance to aminoglycoside and β-lactam antibiotics, chloramphenicol, trimetophrim, sulfonamides, spectinomycin and others (Partridge et al 2009;Moura et al 2009). They can also carry other adaptive genes associated with environmental stresses or open reading frames, coding hypothetical proteins of unknown function (Elsaied et al 2007(Elsaied et al , 2011.…”