High prevalence of IncP-1 plasmids and IS1071insertion sequences in on-farm biopurification systems and other pesticide-polluted environments

Abstract

Mobile genetic elements (MGEs) are considered as key players in the adaptation of bacteria to degrade organic xenobiotic recalcitrant compounds such as pesticides. We examined the prevalence and abundance of IncP-1 plasmids and IS1071, two MGEs that are frequently linked with organic xenobiotic degradation, in laboratory and field ecosystems with and without pesticide pollution history. The ecosystems included on-farm biopurification systems (BPS) processing pesticide-contaminated wastewater and soil. Comparison of IncP-1/IS1071 prevalence between pesticide-treated and nontreated soil and BPS microcosms suggested that both IncP-1 and IS1071 proliferated as a response to pesticide treatment. The increased prevalence of IncP-1 plasmids and IS1071-specific sequences in treated systems was accompanied by an increase in the capacity to mineralize the applied pesticides. Both elements were also encountered in high abundance in field BPS ecosystems that were in operation at farmyards and that showed the capacity to degrade/mineralize a wide range of chlorinated aromatics and pesticides. In contrast, IS1071 and especially IncP-1, MGE were less abundant in field ecosystems without pesticide history although some of them still showed a high IS1071 abundance. Our data suggest that MGE-containing organisms were enriched in pesticide-contaminated environments like BPS where they might contribute to spreading of catabolic genes and to pathway assembly.

Shifts in Abundance and Diversity of Mobile Genetic Elements after the Introduction of Diverse Pesticides into an On-Farm Biopurification System over the Course of a Year

“…The very high relative abundances of the promiscuous IncP-1 plasmids detected in the BPS are comparable to those seen with other "hot spots" of horizontal gene transfer such as manure, sewage, or polluted river sediments (39,40). Our data confirm the results of two recent studies using TC-DNA from different BPS which also found an unusually high abundance of IncP-1 plasmids in the BPS (15,37). Interestingly, the abundance of IncP-1 plasmids seemed to be increased in BPS bacteria, likely in response to the exposure to different types and concentrations of pesticides as recently reported by Jechalke et al (14).…”

“…In accordance with previous findings (14,37), we hypothesize that temporal changes in the abundance and diversity of MGEs in an on-farm BPS might be caused by changes in the composition and concentration of the pesticides added to the BPS over the course of the agricultural season. To test our hypothesis and to provide the first more comprehensive view on the mobilome of BPS bacterial communities, cultivation-independent techniques were applied to investigate shifts in the abundance and diversity of the MGEs of bacterial communities of a BPS in operation on a farm in Kortrijk, Belgium, over the course of the agricultural season of 2011.…”

“…high abundance of IncP-1, IncP-7, and IncP-9 plasmids and insertion sequence (IS) elements typically associated with degradative genes (15,37). Here we monitored fluctuations of a range of different plasmids, integrase genes of class 1 and class 2 integrons, and sulfonamide and streptomycin resistance genes at three times during the agricultural season: before the pesticide spraying season (March), at the height of the spraying season (July), and after the spraying season (September).…”

“…BPS act like biofilters in which the filter matrix (biomix) is composed of a mixture of different adsorbing materials, such as peat, straw, and topsoil (2), and contain microorganisms carrying mobile genetic elements (MGEs) that harbor genes involved in biodegradation of xenobiotic compounds (3,37). Although it is well known that biodegradation is the main process in the removal of xenobiotic compounds from the environment (3), abiotic factors such as temperature and concentration of pesticides can substantially influence their degradation (4).…”

“…Specifically, IncP-1 plasmids are highly promiscuous plasmids and were reported to carry genes coding for enzymes involved in degradation of different xenobiotic compounds (10)(11)(12). Correspondingly, it has been observed that prolonged exposure to pesticides enriches for bacterial populations carrying IncP-1 plasmids (13,14,37).…”