Influences of hexafluoropropylene oxide (HFPO) homologues on soil microbial communities

Highlights

• HFPO affected microbial density and community structure and nitrifying activity.

• HFPO-DA had a lasting and suppressive effect on AOB and nitrifying activity.

• AOB were more sensitive to HFPO.

Abstract

Hexafluoropropylene oxide (HFPO) homologues, as emerging perfluoroalkyl substances (PFASs) to replace legacy PFASs, have wide applications in the organofluorine industry and have been detected in the global environment. However, it is still unclear what effect HFPO homologues will exert on microbial abundance, community structure and function. The objective of this study was to assess potential impacts of HFPO homologue acids on archaea, bacteria, and ammonia-oxidizing archaea (AOA) and bacteria (AOB) in the soil environment. Grassland soil microcosms were supplemented with low (0.1 mg/kg) or high (10 mg/kg) dosages of dimer, trimer and tetramer acids of HFPO (HFPO-DA, HFPO-TA, and HFPO-TeA), respectively. The amendment of HFPO homologues acids initially decreased the abundance of archaea and bacteria but increased them in the later period. The addition of HFPO homologues acids raised AOA abundance but restrained AOB growth during the whole incubation. AOA and AOB community structures showed considerable variations. Potential nitrifying rate (PNR) showed an increase in the initial period followed by a decline in the later period. HFPO-DA had a lasting and suppressive effect on AOB and PNR even at a nearly environmental level. Overall, HFPO homologues with different carbon chain lengths had different impacts on soil microbial community and ammonia oxidation.

Introduction

With the phase-out of legacy perfluoroalkyl substances (PFASs), PFASs with shorter carbon chain length and containing ethers have found increasing applications, and have therefore been released into the environment (Wang et al., 2013, 2015, 2017, 2019). Hexafluoropropylene oxide (HFPO) homologues belong to the perfluoro-ether carboxylic acids and have replaced perfluorooctanoic acid (PFOA) as processing aids (Heydebreck et al., 2015; Pan et al., 2017; Song et al., 2018). They play a critical role as additives in the manufacture of fluorine polymers (Song et al., 2018), so fluorine factories are major sources of HFPO homologues pollution (Brandsma et al., 2019). HFPO homologues include dimer, trimer and tetramer acids of HFPO (HFPO-DA, HFPO-TA, and HFPO-TeA) (Song et al., 2018). HFPO homologues are attracting mounting attention because of their ubiquitous detection in multimedia environmental samples (Brandsma et al., 2019; Cui et al., 2018; Pan et al., 2017, 2018), and their similarity to legacy PFASs in terms of persistence and toxicity (Bao et al., 2018a; Brandsma et al., 2019; Cui et al., 2018; Li et al., 2019). The reported highest concentration of HFPO-DA in surface water near fluorine factories is 631 ng/L in the USA, 108 ng/L in Germany, 812 ng/L in The Netherlands, and 3830 ng/L in China (Gebbink et al., 2017; Heydebreck et al., 2015; Sun et al., 2016a). In China, HFPO-TA has been reported to have reached 68 500 ng/L (maximum) in a river downstream of a fluorine plant, 1510 ng/L (median) in wild common carp, and 2.93 ng/L (median) in the sera of residents (Pan et al., 2017). HFPO-TeA ranged from <LOQ (limit of quantification) to 42.6 ng/g in 2014 and <LOQ to 363 ng/g in 2016 in sediment (Song et al., 2018). HFPO homologues have even exhibited greater risks than their predecessor PFOA, owing to their stronger disruptive effects on adipogenic activity related with hepatoxicity and estrogenic effects in vitro and vivo experiments (Li et al., 2019; Song et al., 2018; Xin et al., 2019).

Since HFPO homologues are frequently detected in surface water near fluorine plants, it is reasonable to speculate that HFPO homologues can also exist in soil via air transportation, water penetration and surface runoff (Brandsma et al., 2019; Cai et al., 2019). Therefore, soil could be an important sink for HFPO homologues. Soil microbial density and community structure are sensitive to the pressure of legacy PFASs (Bao et al., 2018b; Li et al., 2017; Qiao et al., 2018). In addition, PFASs greatly altered sediment microbial community (Zhang et al., 2017). PFOA could induce a long-term change of microbial community in activated sludge (Yu et al., 2018). Nonetheless, it is still unknown whether HFPO homologues can alter microbial community in natural or man-made environment. In addition, microorganisms are a crucial participator in nitrogen transformation (Ju et al., 2017). Ammonia oxidation is the first and rate-determining step in nitrification and it is important in soil nitrogen transformation (Wan et al., 2014). Both ammonia-oxidizing bacteria (AOB) and archaea (AOA) assign the role of ammonia oxidization. These two ammonia-oxidizing microorganisms (AOMs) harbor the ammonia monooxygenase (amoA) gene catalyzing ammonia conversion. AOA usually play a dominant role in salty, acid and nitrogen deficient environments (Nicol et al., 2008; Sterngren et al., 2015). Ammonia oxidation is sensitive to many pollutants such as heavy metal, antibiotics, pesticides and poly brominated diphenyl ethers (Du et al., 2018; Xia et al., 2019; Wang et al., 2018a), yet the effect of HFPO homologues on soil nitrification remains unclear.

Previous studies have indicated that emerging HFPO homologues influenced eukaryotic cells (e.g., zebrafish, mice and human cells) and caused estrogen disruption and hepatotoxicity (Li et al., 2019; Xin et al., 2019). HFPO homologues with longer carbon chains exhibit a strong binding affinity with estrogen receptors and peroxisome proliferator-activated receptors (Li et al., 2019; Xin et al., 2019). In addition, legacy PFASs of various chain lengths could have different consequences for bacteria in terms of membrane damage, oxidative stress, cell lesion and DNA damage (Nobels et al., 2010). Quorum sensing in bacteria was found to increase when exposed to PFASs with longer carbon chains due to the increase in cell membrane permeability (Fitzgerald et al., 2018; Mulkiewicz et al., 2007). Therefore, we hypothesized that HFPO homologues of different carbon chain lengths might cause different disturbances to soil communities. In this context, the objective of the current work was to explore the effects of different HFPO homologues on the microbial community and ammonia oxidation in soil.