Wastewater Irrigation Increases the Abundance of Potentially Harmful Gammaproteobacteria in Soils in Mezquital Valley, Mexico

Abstract

eWastewater contains large amounts of pharmaceuticals, pathogens, and antimicrobial resistance determinants. Only a little is known about the dissemination of resistance determinants and changes in soil microbial communities affected by wastewater irrigation. Community DNAs from Mezquital Valley soils under irrigation with untreated wastewater for 0 to 100 years were analyzed by quantitative real-time PCR for the presence of sul genes, encoding resistance to sulfonamides. Amplicon sequencing of bacterial 16S rRNA genes from community DNAs from soils irrigated for 0, 8, 10, 85, and 100 years was performed and revealed a 14% increase of the relative abundance of Proteobacteria in rainy season soils and a 26.7% increase in dry season soils for soils irrigated for 100 years with wastewater. In particular, Gammaproteobacteria, including potential pathogens, such as Pseudomonas, Stenotrophomonas, and Acinetobacter spp., were found in wastewater-irrigated fields. 16S rRNA gene sequencing of 96 isolates from soils irrigated with wastewater for 100 years (48 from dry and 48 from rainy season soils) revealed that 46% were affiliated with the Gammaproteobacteria (mainly potentially pathogenic Stenotrophomonas strains) and 50% with the Bacilli, whereas all 96 isolates from rain-fed soils (48 from dry and 48 from rainy season soils) were affiliated with the Bacilli. Up to six types of antibiotic resistance were found in isolates from wastewater-irrigated soils; sulfamethoxazole resistance was the most abundant (33.3% of the isolates), followed by oxacillin resistance (21.9% of the isolates). In summary, we detected an increase of potentially harmful bacteria and a larger incidence of resistance determinants in wastewater-irrigated soils, which might result in health risks for farm workers and consumers of wastewater-irrigated crops.

Impacts of Long-Term Irrigation of Domestic Treated Wastewater on Soil Biogeochemistry and Bacterial Community Structure

“…It is imperative to note that despite the recent interest in the impacts of TWW irrigation on soils (17,31), rarely has the impact of land application of wastewater been correlated to both the biogeochemistry and associated soil microbiota that underpin biogeochemical processes. This is especially true for the bacterial NO 3Ϫ reducers, which likely are one of the main guilds mediating N sequestration in such TWW-impacted environments.…”

“…Most notably, land application of TWW has the potential to transfer heavy metals (14), pharmaceuticals (15), and even pathogens (16) in the environment and into the food chain (17). In fact, several studies have shown that nutrients, including total carbon (TC), total nitrogen (TN), and soil microbial quotient (the ratio of microbial biomass carbon [MBC] to soil total organic C) remain higher in soils irrigated (IR) with TWW (4,5,9,18,19).…”

“…Even the studies that have attempted to assess the impact of land application of wastewater have primarily focused on the enzymatic activity of soil microorganisms, the fate and transport of pathogenic microorganisms from the irrigated wastewater into the soils, or the characterization of antibiotic resistance in bacteria isolated from the irrigated soils (17,(30)(31)(32). To address the impact of TWW irrigation on soil microorganisms, Hidri and colleagues (33) utilized automated ribosomal intergenic spacer analysis (ARISA), and more recently Frenk et al (31) and Broszat et al (17) used 454 massively parallel tag sequencing (MPTS) of small-subunit (SSU) rRNA genes to show that the soil bacterial communities were indeed impacted by wastewater irrigation such that irrigation caused an increase in the relative abundances of potentially pathogenic gammaproteobacterial assemblages within the TWWirrigated soils.…”

Assessing Technical and Economic Feasibility of Complete Bioremediation for Soils Chronically Polluted with Petroleum Hydrocarbons

“…The consortium was composed of two strains belonging to Pseudomonas and three strains from Acinetobacter genus. Acinetobacter strains are among the most abundant and ubiquitous microorganisms in soils and wastewater [34][35][36][37][38][39]. Notably, Acinetobacter strains are ubiquitous in oil-contaminated environments [40][41][42].…”

Antimicrobial Resistance Genes and Wastewater Treatment

“…Some studies have observed an increase in soil microbial activity and biomass after irrigation by treated wastewater as shown by a shift in the composition of soil bacterial communities (Oved et al, 2001;Broszat et al, 2014). However, recent studies have observed no significant impact on AR in the wastewater-irrigated soil microbiome (Gatica and Cytryn, 2013;Negreanu et al, 2012).…”