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Genome Sequencing Reveals the Environmental Origin of Enterococci and Potential Biomarkers for Water Quality Monitoring
Weigand, M., N. Ashbolt, K. Konstantinidis, AND J. Santodomingo. Genome Sequencing Reveals the Environmental Origin of Enterococci and Potential Biomarkers for Water Quality Monitoring. ENVIRONMENTAL SCIENCE & TECHNOLOGY. ACS Publications, Washington, DC, 48(7):3707-3714, (2014).
Towards a more complete characterization of the total genetic and ecological diversity of E. faecalis and improved discrimination of fecal indicator organisms, we sequenced 11 isolates recovered from geographically disparate watersheds that are impacted by municipal wastewater treatment plants or agricultural industry that exhibited colony morphology typical for grown on enterococci selective media and compared them with 59 publically available genome sequences of enteric isolates, both commensal and pathogenic. We hypothesized that, despite strong phylogenetic cohesion, discrete gene signatures facilitate habitat specialization and thus, differentiate isolates of environmental and enteric origin. These gene signatures would also provide insights into the evolutionary history and speciation process of E. faecalis, which will be applicable to additional fecal indicator bacteria, as well as the molecular mechanisms of gut colonization.
Enterococci are common members of the gut microbiome and frequent causative agents of nosocomial infection. Because of their enteric lifestyle and ease of culturing, enterococci have been used worldwide as indicators of fecal pollution of waters. However, enterococci were recently shown to persist in environmental habitats, often in the absence of fecal input, potentially confounding water quality assays. Toward resolving this issue and providing a more complete picture of the natural diversity of enterococci, 11 isolates of Enterococcus faecalis recovered from freshwater watersheds (environmental) were sequenced and compared to 59 available enteric genomes. Phenotypic testing and core genome phylogeny revealed that the environmental E. faecalis were indistinguishable from their enteric counterparts. However, distinct environment- and host-specific gene signatures, encoding accessory nutrient utilization pathways, were detected among the variable E. faecalis genes. For instance, a nickel uptake operon was enriched in the environmental genomes and undetectable in human gut metagenomes, consistent with its importance in extra-enteric habitats. Further, genes for utilization of sugars thought to be abundant in the gut such as lactose were enriched in enteric genomes. The distribution and phylogeny of identified gene signatures indicated that E. faecalis preferably resides in extra-enteric habitats and secondarily adapts to the gastrointestinal tract, challenging prevailing views of enterococci ecology. Thus, it appears that habitat-specific genes change faster than core genome phylogeny and such genes appear to represent robust biomarkers for discriminating fecal contaminants from innocuous, environmentally-adapted close-relatives, providing means for improved microbial water quality monitoring over current practices.