Community-level and function response of photoautotrophic periphyton exposed to oxytetracycline hydrochloride

Highlights

• Effects of OTC ecotoxicology on periphyton were first time studied.

• Low OTC concentrations stimulated an epilithon biomass increase.

• High OTC concentrations caused release of nutrients in the short term.

• Periphyton function recovered rapidly after subjection to antibiotic stress.

Abstract

Periphyton is considered important for removal of organic pollutants from water bodies, but knowledge of the impacts of antibiotics on the community structure and ecological function of waterbodies remains limited. In this study, the effects of oxytetracycline hydrochloride (OTC) on the communities of photoautotrophic epilithon and epipelon and its effect on nitrogen and phosphorus concentrations in the water column were studied in a 12-day mesocosm experiment. The dynamics of nitrogen and phosphorus concentrations in the epipelon and epilithon experiment showed similar patterns. The concentrations of total nitrogen, dissolved total nitrogen, ammonium nitrogen, total phosphorus and dissolved total phosphorus in the water column increased rapidly during the initial days of exposure, after which a downward trend occurred. In the epilithon experiment, we found that the photosynthesis (Fv/Fm) and biomass of epilithon were significantly (P < 0.05) stimulated in the low concentration group. Contrarily, growth and photosynthesis (Fv/Fm) were significantly (P < 0.05) reduced in the medium and high concentration group. We further found that the photosynthetic efficiency of photoautotrophic epilithon was negatively correlated with the concentrations of nitrogen and phosphorus in the water column (P < 0.05). Principal coordinate analysis (PCoA) showed that the communities of epilithic algae in the control group and in the low concentration group were significantly (P < 0.05) different from that of the high concentration group during the initial 4 days. After 8 days’ exposure, all groups tended to be similar, indicating that epilithon showed rapid adaptability and/or resilience. Similar results were found for the relative abundance of some epilithic algae. Our findings indicate that the biofilm system has strong tolerance and adaptability to OTC as it recovered fast after an initial suppression, thus showing the important role of periphyton in maintaining the dynamic balance of nutrients with other processes in aquatic ecosystems.

Introduction

Extensive use of antibiotics in human medicine, animal husbandry and aquaculture has greatly increased the presence and concentrations of antibiotics in the natural environment (Xu et al., 2007; Klaus, 2009). Globally, the consumption of antibiotics increased by 65% between 2000 and 2015, from 21.1 to 34.8 billion daily doses (DDDs), and it is predicted that global antibiotic use in 2030 will be 200% higher than the 42 billion DDDs in 2015 (Klein et al., 2018). In China, the total use of antibiotics reached 162,000 t in 2013 (Zhang et al., 2015), and a study based on six-years (2012–2017) of surveillance sales records showed that the daily doses (DID) per 1000 inhabitants in Shandong Province, China, had increased from 11.4 to 17.4 (Song et al., 2020). Due to improper use and illegal discharges, antibiotics may enter surface water systems where they may become a serious threat to the aquatic ecosystems and their stability (Homem and Santos, 2011; Wang et al., 2017; Minh et al., 2009; Yiruhan et al., 2010). Furthermore, antibiotics can be transmitted to and gradually enriched in the food chain, presenting a human health risk (Golet et al., 2002). Therefore, it is of paramount importance to assess the possible risks to the aquatic environment caused by antibiotics and to develop effective approaches to remove such risks (Nie et al., 2010; Martins et al., 2012).

Tetracycline (TCs), such as oxytetracycline hydrochloride (OTC), which can inhibit the protein synthesis of pathogenic microorganisms, is one of the most widely used antibiotics in human disease treatment, animal husbandry and aquaculture (Pan et al., 2011; Chopra, 2001). Studies have reported that TCs can be hydrolysed or photolysed after its discharge into water (Perez et al., 2005), and the toxicity of intermediate degradation products is much higher than that of TCs itself as these products may degrade to different segments with potentially combined synergistic or antagonistic effects (Guo and Chen, 2012). For example, levofloxacin, norfloxacin and enoxacin are the main toxic degradation TCs products that affect aquatic organisms (Robinson et al., 2005; Paul et al., 2007; Gonzdlez-Pleiter et al., 2013). A study by Guo and Chen (2012) showed that degraded chlortetracycline was more toxic for the growth and chlorophyll-a accumulation of Scenedesmus obliquus (a green algae) than chlortetracycline itself. OTC is a compound that can be accumulated in aquatic organisms and may threaten the physiological system by hindering the normal biological regulation process (Jonsson et al., 2001). Due to the long degradation time of oxytetracycline in water, it not only has acute toxic effects on aquatic organisms but also chronic effects at long-term exposure (Wollenberger et al., 2000). Although the number of studies on the ecotoxicological effects of OTC on aquatic organisms at individual level is increasing (Kolar et al., 2014; Gusso et al., 2021), the impact of OTC at the community level of aquatic flora has not been extensively investigated.

Periphyton are complex conglomerations of algae, bacteria, fungi, protozoa and other micro and meso-organisms (Wu et al., 2012; Coenye and Nelis, 2010; Azim and Asaeda, 2005). They have multiple ecological functions and may change the physical and chemical microhabitats and thereby further affect larger-scale aquatic ecosystem processes (Battin et al., 2003). Studies have shown that periphyton play an important role in the process of water purification by effectively assimilating nitrogen, phosphorus, nitrate, ammonia, heavy metals and other pollutants in the water column (Arnon et al., 2007; Writer et al., 2011; Kang et al., 2018; Zhao et al., 2018). Periphyton can also create a biofilm on the sediment surface and in this way reduce the release of nutrients and gasses from the sediment to the water column (Castro et al., 2017). Since periphyton are important photoautotrophic organisms, changes in the periphyton community will also affect the upper trophic levels (Claudio and Aoyama, 2007) and, with it, the function and stability of local habitats (Salmaso, 2010). In addition, periphyton can respond quickly to antibiotics and other environmental pollutants, and accordingly be indicators of water quality changes (Viviana et al., 2020; Lawrence et al., 2015). Studies have shown that sulfa antibiotics can reduce the diversity of diatom assemblages in periphyton and induce diatom deformities (e.g. Kergoat et al., 2021). Another study by Johansson (2014) showed that 9000 nmol·L⁻¹ ciprofloxacin and sulfamethoxazole did not significantly change the part of algae of the community composition of marine periphyton. However, over-all, our understanding of the effects of antibiotics on the community and function of periphyton is still insufficient.

We designed two mesocosm experiments to investigate the effects of OTC on the growth and community-level response of periphyton as well as on the dynamics of nitrogen and phosphorus in the water column. We hypothesised that: 1) the community structure and function of periphyton would be affected by OTC exposure, producing increased abundance of endogenous nutrients in the water column, but that 2) the function of periphyton would show relatively fast recovery due to their capacity of maintaining community stability (such as regulation of diversity and dominant species in a changing environment), which would re-establish the nutrient removal capacity.