Distribution of microbial communities in metal-contaminated nearshore sediment from Eastern Guangdong, China

Highlights

• Richness and diversity were higher on Lianjiang and Rongjiang River mouths.

• Proteobacteria and Gammaproteobacteria were the most abundant phyla and class.

• About 39% of the nearshore sediments in eastern Guangdong were contaminated.

• Nitrospirae and OD1 had significant correlation with all metals except Cr.

• Planctomycetes and Verrucomicrobia maybe playing key roles in carbon biogeochemical.

Abstract

Nearshore environments are a critical transitional zone that connects the marine and terrestrial/freshwater ecosystems. The release of anthropogenic chemicals into nearshore ecosystems pose a human and environmental health risk. We investigated the microbial diversity, abundance and function in metal-contaminated sediments collected from the Rongjiang, Hanjiang and Lianjiang River estuaries and adjacent coastal areas using high throughput sequencing. The concentration of nutrients (NO₃-N, NO₂-N, NH₄-N, PO₄-P) and metal (Cu, Zn, Cd, Pb, As, Hg) contaminants were higher at the mouth of the rivers compared to the coastal lines, and this was confirmed using cluster analysis. Estimates obtained using geoaccumulation index showed that about 38.9% of the sites were contaminated with Pb and the pollution load index showed that sediment from the mouth of Hanjiang River Estuary was moderately polluted with metals. In the nearshore sediment samples collected, Proteobacteria, Bacteroidetes, Planctomycetes, Chloroflexi, Acidobacteria were the dominant phylum with relative abundances of 46.6%, 8.05%, 6.47%, 5.26%, and 4.59%, respectively. There was no significant correlation between environmental variables and microbial abundance and diversity except for total organic carbon (TOC) (diversity; r = 0.569, p < 0.05) and Cr (diversity; r = 0.581, p < 0.05). At phyla level, Nitrospirae had a significant negative correlation with all metals except Cr, while OD1 had a significant positive correlation with all the metals. Overall, changes in nearshore sediment microbial communities by environmental factors were observed, and these may affect biogeochemical cycling.

Introduction

Nearshore environments are centers of high productivity and diversity that offer critical ecological services such as nutrient cycling and mineralization of organic matter (Cleary et al., 2017). With nearly two billion people living less than 100 km from the coastline, nearshore environments are threatened by anthropogenic pressure (Zhu et al., 2017). Unfortunately, without drastic intervention, deterioration of nearshore ecosystems is probably going to exacerbate as human populations and industrial activities in coastal areas increase. Discharges from anthropogenic activities (such as aquaculture, agriculture, mining, electronic manufacturing, and sewage treatment) may increase metal and inorganic nutrient contamination in nearshore ecosystems which may disturb benthic bacterial communities (Shi et al., 2018). Benthic bacterial communities in nearshore environments play an important role in biogeochemical processes and ecological mechanisms that maintain ecosystem functions (Bowman and McCuaig, 2003). This is because benthic microbial communities regulate the cycling of carbon, nitrogen, sulfur, phosphorus, and metals in nearshore environments (Chen et al., 2019). However, benthic bacteria require metals for survival and growth but at higher concentrations metals can cause adverse effects. Hence, understanding the response of microbial communities to environmental variables as well as their spatial distribution is essential for effective management of nearshore ecosystems.

There is little information available on the relative contribution of environmental variables and spatial factors to microbial abundance and diversity probably because of the environmental heterogeneity of nearshore ecosystems. Environmental conditions in nearshore ecosystems are heterogeneous because they experience frequent anthropogenic disturbances and sharp environmental gradients due to dynamic interactions between terrestrial and oceanic processes. Previous studies on the spatial variation of distribution of bacterial communities focused on the water column even though sediments are an important habitat of bacterial communities involved in ecosystem services as well as a sink of metal contaminants. For example, Yu et al. (2017) found that the distribution of microbial communities in water column along Xiaoqing River to Laizhou Bay followed a distinct geographic pattern, and this suggested that the microbial communities had a different function in the biogeochemical processes. Hence, microbial communities in nearshore sediments may have complex biogeographic variations due to spatial factors and changes in environmental conditions (Martiny et al., 2011).

A few studies investigated shifts in bacterial communities in sediments contaminated with hydrocarbons (Paissé et al., 2008), polychlorinated biphenyls (Quero et al., 2015), polyaromatic hydrocarbons, nonylphenols and bisphenol A (Zoppini et al., 2018). However, the few studies that are available found conflicting relationships between metal pollution and bacterial community structures and diversity, mainly because of the differences in the ecological data provided by the quantitative methods employed (Gillan et al., 2005; Nogales et al., 2011). For example, a study using fluorescent in situ hybridization in highly polluted sediment found a negative correlation between Cd, Cu and Zn and the relative abundance of Bacteroidetes (Gillan et al., 2005). However, another study that used 16s rDNA and denaturing gradient gel electrophoresis in less-polluted marine sediments only found a significant correlation between Bacteroidetes and Cd (Powell et al., 2003). Hence, the applicability of microbial community characterization in understanding and modelling ecological processes in metal-contaminated nearshore ecosystems remains unresolved (Bier et al., 2015; Nogales et al., 2011).

Marine pollution in eastern Guangdong is an issue of major concern because the coastal waters are a major habitat for the near threatened Indo-Pacific humpback dolphins (Sanganyado et al., 2018; Shi et al., 2018). Rapid urbanization and industrialization upstream the Lianjiang, Rongjiang, and Hanjiang Rivers in eastern Guangdong contribute to the discharge of potentially toxic elements and inorganic nutrients into their respective estuaries and the adjacent coastal waters, respectively (Qiao et al., 2013b). Besides differences in upstream activities, the three rivers have different hydrological and hydrodynamic characteristics, which makes them proper study sites for understanding the effect of anthropogenic activities in nearshore ecosystems. We hypothesized that the relative abundance, diversity, and function of bacterial communities were modified by potentially toxic metals and that the magnitude of the effects depended on the nature and concentration of the metal in the sediment. Furthermore, although earlier studies showed that inorganic nutrients influence bacterial community structure and function, their overall contribution compared to metals has not yet been systematically investigated. For this purpose, nearshore sediments from estuaries and coastal zones in Eastern Guangdong, China were used to assess whether the bacterial community structure in metal-contaminated sediment varied along contaminant (metals and inorganic nutrients) gradients, and to evaluate whether geographic distance contributed to the spatial variation of bacterial communities in nearshore sediments.