Microbial community structure and function in sediments from e-waste contaminated rivers at Guiyu area of China

Highlights

• River sediments from Guiyu were severely polluted by TOPs and heavy metals.

• Deltaproteobacteria dominated the sediment microbial assemblages.

• Some of the dominant genera might harbor pathways for TOPs degradation.

• TOPs contributed more to community structure and function than heavy metals.

• BaP, available lead and EC were the key contributors.

Abstract

The release of toxic organic pollutants and heavy metals by primitive electronic waste (e-waste) processing to waterways has raised significant concerns, but little is known about their potential ecological effects on aquatic biota especially microorganisms. We characterized the microbial community composition and diversity in sediments sampled along two rivers consistently polluted by e-waste, and explored how community functions may respond to the complex combined pollution. High-throughput 16S rRNA gene sequencing showed that Proteobacteria (particularly Deltaproteobacteria) dominated the sediment microbial assemblages followed by Bacteroidetes, Acidobacteria, Chloroflexi and Firmicutes. PICRUSt metagenome inference provided an initial insight into the metabolic potentials of these e-waste affected communities, speculating that organic pollutants degradation in the sediment might be mainly performed by some of the dominant genera (such as Sulfuricurvum, Thiobacillus and Burkholderia) detected in situ. Statistical analyses revealed that toxic organic compounds contributed more to the observed variations in sediment microbial community structure and predicted functions (24.68% and 8.89%, respectively) than heavy metals (12.18% and 4.68%), and Benzo(a)pyrene, bioavailable lead and electrical conductivity were the key contributors. These results have shed light on the microbial assemblages in e-waste contaminated river sediments, indicating a potential influence of e-waste pollution on the microbial community structure and function in aquatic ecosystems.

Introduction

Discarded electrical and electronic products are entering the electronic waste (e-waste) stream in a growing flood, due to the rapid development of the electronics industry (Ongondo et al., 2011). Reportedly at least 20 to 50 million tons of e-waste are generated annually worldwide (UNEP, 2005), with a growth rate of about 4% (Robinson, 2009). Some less developed countries in Asia, China in particular, have been receiving substantial amount of globally generated e-waste for recycling due to lower local labor costs and less stringent environmental regulations (Wong et al., 2007b; Zhang et al., 2012). However, the unregulated, primitive e-waste processing activities have led to the release of toxic metals (e.g., copper, zinc, cadmium and lead) and toxic organic pollutants (TOPs) (e.g., polycyclic aromatic hydrocarbons [PAHs], polychlorinated biphenyls [PCBs] and polybrominated diphenyl ethers [PBDEs]) into local aquatic and terrestrial ecosystems (Fink et al., 2000, Wang et al., 2011). Specifically, previous investigations have reported elevated levels of metals and toxic organic substances in the waters and sediments downstream the e-waste recycling areas (Wong et al., 2007a, Wong et al., 2007b). The pollution of aquatic environments imposes a major threat to local ecosystems and human health.

The microorganisms in sediments play a significant role in the biogeochemical cycling of elements, food webs and the functioning of aquatic ecosystems (Nealson, 1997). The benthic prokaryotes in various habitats have been investigated by culture-independent molecular approaches, revealing that sediment microbial assemblages are more diverse than those of any other environment (Lozupone and Knight, 2007, Zinger et al., 2011). This may be attributable to the high heterogeneity of the sediment (in terms of environmental gradients and biogeochemical processes), which may provide an enhanced number of niches, allowing the coexistence of more diversified assemblages of organisms contributing to ecosystem stability (Wittebolle et al., 2009). On the other hand, many inland and coastal aquatic environments are substantially perturbated by human activities, leading to eutrophication and deterioration of natural systems. The vast metabolic potentials of sediment microorganisms are crucial for the transformation, degradation or detoxification of pollutants such as heavy metals and toxic organic compounds. Furthermore, the structure and metabolic activities of microbial communities are a sensitive and comprehensive indicator of residual toxicity (White et al., 1998, Watanabe and Hamamura, 2003, Huang et al., 2016). Consequently, a thorough knowledge of the ecology of the indigenous microbial assemblages will help predict the natural attenuation processes in the sediment and the recovery stage of aquatic ecosystems.

While the effects of heavy metals and TOPs on microorganisms in the environment have recently received considerable attentions (Jackson et al., 2015, Dombrowski et al., 2016), the ecological consequences of the complex combined pollution associated with e-waste recycling on microbial assemblages in natural settings, especially aquatic environments, remain largely unknown. A recent attempt has investigated the composition and diversity of microbial communities in soils at multiple e-waste recycling sites (Liu et al., 2015). Although documenting drastic shifts of community members largely driven by soil physiochemical variables and organic pollutants, such findings are confined to the community structure at these highly contaminated sites. Furthermore, it remains unclear how community functions are affected by and respond to the stressful conditions caused by the complex combined pollution of heavy metals and TOPs.

In the past two decades, many functional microbes (e.g., Pseudomonas spp., Sphingomonas spp. and Ochrobactrum spp.) degrading TOPs and resistant and tolerant to heavy metals have been isolated from the relevant e-waste polluted environments (An et al., 2011, Shi et al., 2013), and the subsequent experiments have uncovered molecular mechanisms of microbial degradation and resistance in these species (Field and Sierra-Alvarez, 2008, Haritash and Kaushik, 2009, Robrock et al., 2009). We hypothesized that the complex combined pollution associated with primitive e-waste processing may exert strong selective pressure on the microflora in the aquatic sediments, resulting in that microbes resistant and tolerant to heavy metals and degrading toxic organic compounds become dominant lineages and then the community function is changed to response to the complex combined pollution. Here we report an in-depth survey of the microbial assemblages in a series of sediments collected at cross sections from different locations along two rivers affected by extensive e-waste recycling activities. The objectives of this study were 1) to examine the composition and diversity of microbial communities in the e-waste contaminated river sediments; 2) to explore how community structure and function may be influenced by the complex combined pollution. The results provide insights into the potential ecological impacts of e-waste pollution on the microbial community structure and functions of sediments in these perturbated aquatic ecosystems.