Abstract
Perfluoroalkyl and polyfluoroalkyl substances (PFAS) are environmental contaminants of concern. We previously described biodegradation of two PFAS that represent components and transformation products of aqueous film-forming foams (AFFF), 6:2 fluorotelomer sulfonamidoalkyl betaine (6:2 FTAB) and 6:2 fluorotelomer sulfonate (6:2 FTSA), by Gordonia sp. strain NB4-1Y. To identify genes involved in the breakdown of these compounds, the transcriptomic response of NB4-1Y was examined when grown on 6:2 FTAB, 6:2 FTSA, a non-fluorinated analog of 6:2 FTSA (1-octanesulfonate), or MgSO4, as sole sulfur source. Differentially expressed genes were identified as those with ± 1.5 log2-fold-differences (± 1.5 log2FD) in transcript abundances in pairwise comparisons. Transcriptomes of cells grown on 6:2 FTAB and 6:2 FTSA were most similar (7.9% of genes expressed ± 1.5 log2FD); however, several genes that were expressed in greater abundance in 6:2 FTAB treated cells compared to 6:2 FTSA treated cells were noted for their potential role in carbon–nitrogen bond cleavage in 6:2 FTAB. Responses to sulfur limitation were observed in 6:2 FTAB, 6:2 FTSA, and 1-octanesulfonate treatments, as 20 genes relating to global sulfate stress response were more highly expressed under these conditions compared to the MgSO4 treatment. More highly expressed oxygenase genes in 6:2 FTAB, 6:2 FTSA, and 1-octanesulfonate treatments were found to code for proteins with lower percent sulfur-containing amino acids compared to both the total proteome and to oxygenases showing decreased expression. This work identifies genetic targets for further characterization and will inform studies aimed at evaluating the biodegradation potential of environmental samples through applied genomics.Graphic
Highlights
We have focused on understanding the molecular biology underlying polyfluoroalkyl substances (PFAS) metabolism in the aerobic soil bacterium, Gordonia sp. strain NB4-1Y, with interest in desulfonation reactions that liberate sulfite from 6:2 fluorotelomer sulfonamidoalkyl betaine (6:2 FTAB) and 6:2 fluorotelomer sulfonate (6:2 FTSA) (Shaw et al 2019; Van Hamme et al 2013)
To find coordinated metabolic programs in NB4-1Y, global gene expression in the presence of 6:2 FTAB or 6:2 FTSA was compared to NB4-1Y cultures growing on either MgSO4 as a sulfate rich control, or the sodium salt of 1-octanesulfonate as a non-fluorinated structural analogue of 6:2 FTSA. Through these analyses we identified, for example: 20 genes associated with the transport and metabolism of sulfur compounds more highly expressed with 6:2 FTAB, 6:2 FTSA and OCT compared to MgSO4; three genes associated with carbon–nitrogen bond cleavage more highly expressed with 6:2 FTAB; three alcohol dehydrogenases, three monooxygenases, and three genes associated with acetyl-coenzyme A (CoA) metabolism, as being more highly expressed with 6:2 FTAB and 6:2 FTSA
After NB4-1Y was revived from storage on nutrient agar plates, inoculum cultures were first grown to early stationary phase on 6:2 FTAB, 6:2 FTSA, OCT and MgSO4 prior to inoculating experimental cultures and incubating to mid-logarithmic phase
Summary
Perfluoroalkyl and polyfluoroalkyl substances (PFAS) represent a diverse group of anthropogenic compounds of concern due to their widespread use, potential toxicity (Borg et al 2013; Piekarski et al 2020; Rand and Mabury 2017; Stanifer et al 2018), and resistance to complete removal from sewage (Choi et al 2019; Dimzon et al 2017; Lazcano et al 2019; Stroski et al 2020), drinking water (Hu et al 2016; Li et al 2020; Rahman et al 2014), landfills (Hamid et al 2018; Hepburn et al 2019; Knutsen et al 2019) and environmental reservoirs (Ahrens et al 2015; Ahrens and Bundschuh 2014; Barzen-Hanson et al 2017; Codling et al 2020; Janousek et al 2019; Ross et al 2018). Much of what is known about microbial PFAS metabolism has been derived from chemical analyses of soil, water, groundwater and sediment, mass balance studies of sewage treatment systems (reviewed by Ahrens and Bundschuh 2014; Liu and Mejia Avendano 2013), and in vitro microcosm studies using aerobic (D’Agostino and Mabury 2017; Liu and Liu 2016; Liu et al 2010; Wang et al 2005; Zhang et al 2016) or anaerobic (Zhang et al.2016) mixed cultures taken from these environments. While multi-omic studies examining DNA, RNA, protein and metabolite profiles of microbial communities in PFAS-impacted environments will be valuable for guiding bioremediation, in order to make sense of these complex datasets, fundamental knowledge of the biochemical mechanisms of specific PFAS metabolic steps is needed
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