Dredging mitigates cyanobacterial bloom in eutrophic Lake Nanhu: Shifts in associations between the bacterioplankton community and sediment biogeochemistry

Highlights

• Dredging caused the deficiency of both water and sediment nutrient.

• Sediment biogeochemical processes affected hydrochemistry.

• Dredging decreased diversity and function of bacterioplankton community.

• Dredging caused relatively less competition between bacterioplankton.

• Dredging-driven nutrient deficiency could mitigate cyanobacterial blooms.

Abstract

Cyanobacterial blooms are a worldwide environmental problem, which is partly attributed to their access to excessive nitrogen (N) and phosphorus (P). Preventing the blooms by reducing N and P from internal inputs is viewed as a challenge. To evaluate the effects of dredging on cyanobacterial abundances and bacterioplankton communities, water and sediment samples were collected from eutrophic Lake Nanhu (Wuhan, China) before dredging (2017) and after dredging (2018). After dredging, significant decreases were observed for sediment nutrients (e.g., C, N, and P sources); C-, N-, P-, and S-cycling-related enzyme activity; N- and P-cycling-related gene abundance; microbial abundance; and dramatic changes were observed in the composition of the sediment microbial community. The release rates of nutrient including nitrogen, phosphorus, and organic matter decreased after dredging, and sediment biogeochemistry was closely correlated to nutrient release rates. Additionally, our observations and analyses indicated that the abundance and diversity of the bacterioplankton community decreased significantly, the composition and interaction of the bacterioplankton community dramatically changed, and the bacterioplankton community function (e.g., N, P-cycling-related enzymes and proteins) down regulated after dredging. Water and sediment physicochemical factors explained 72.28% variation in bacterioplankton community composition, and these physicochemical factors were significantly correlated with diversity, composition, and function of bacterioplankton community. Our findings emphasized that cyanobacterial blooms in freshwater ecosystems were closely correlated with noncyanobacterial bacterioplankton that were largely conserved at the phylum level, with Proteobacteria, Actinobacteria, and Bacteroidetes as the main taxa. To our knowledge, this is the first report clarifying the mechanism of cyanobacterial blooms mitigation by dredging, via changing the association between the bacterioplankton community and sediment biogeochemistry. Our findings are of significance and indicate that dredging is effective for mitigating cyanobacterial blooms.

Introduction

Bacterioplankton and phytoplankton are significant and integral components of aquatic microbial food webs by means of carbon source delivery and play critical roles in nutrient (e.g., carbon, nitrogen, and phosphorus sources) biogeochemical cycles (Liu et al., 2015; Isabwe et al., 2018). However, high abundances of bacterioplankton and phytoplankton can lead to algal blooms, which have become increasingly serious environmental problems as a consequence of water eutrophication and climate change (Chen et al., 2016; Te et al., 2017; Feuchtmayr et al., 2019). In freshwater ecosystems, phytoplankton blooms, also known as algal blooms, are dominated by cyanobacteria (which are regarded as one of the most important bacterioplankton types) (Te et al., 2017; Yan et al., 2017; Li et al., 2018; Zhu et al., 2019), and can dramatically alter ambient biogeochemical factors, such as oxygen exhaustion and water opacity (Chen et al., 2016). Cyanobacterial blooms are often closely correlated with other bacterioplankton (Chen et al., 2016; Su et al., 2017; Te et al., 2017), and cyanobacteria could release secondary metabolites (e.g., microcystin, anatoxin-a, and nodularin) into the water (Lezcano et al., 2017; Te et al., 2017; Omidi et al., 2019), which poisons aquatic organisms and threatens the safety of drinking water.

The excess internal and external inputs of phosphorus (P) and nitrogen (N) into water bodies are the main cause of cyanobacterial blooms (Davis et al., 2015; Li et al., 2019). Simultaneous N and P decreases or elimination are significant for bloom control due to N and P co-limitation of primary productivity that have been demonstrated to be a potential key process in freshwater environments (Paerl and Otten, 2016; Wang et al., 2018). A mainstream perspective is that controlling P concentrations in freshwater can successfully curb lake or reservoir eutrophication (Schindler et al., 2016). While water eutrophication cannot be restrained by decreasing N inputs since N₂ fixation can offset N losses (Schindler et al., 2008; Wang et al., 2018). However, this view has been challenged and demonstrated to be incorrect for some eutrophic waters where N could also be significant factor for the control of water eutrophication (Paerl et al., 2010; Horst et al., 2014; Li et al., 2018). Controlling N and P inputs into freshwater is still an effective way to mitigate cyanobacterial blooms.

N and P concentrations, especially P, present periodic changes in freshwater ecosystems (Jing et al., 2015; Chen et al., 2019; Wang et al., 2019a). The external inputs of N and P can be controlled by limiting discharges of untreated sewage water. The internal inputs of N and P can be controlled by using dredging (Jing et al., 2015). Removal of sediments, also known as dredging, has been widely acknowledged as an effective measure for controlling cyanobacterial blooms (Lürling and Faassen, 2012; Jing et al., 2015; Bormans et al., 2016; Liu et al., 2016). Such large-scale anthropogenic disturbances ultimately profoundly improve water quality to decrease water turbidity, nutrients (e.g., C, N, and P sources), toxins, and heavy metal in both water and sediment (Jing et al., 2015; Ragnarsson et al., 2015; Oldenborg and Steinman, 2019). Previous researches have reported that dredging can significantly affect the composition of the sediment microbial community (Edlund and Jansson, 2006; Chiellini et al., 2013; Zhang et al., 2017), and thus could affect nutrient transfer from sediment to water. However, the mechanism of cyanobacterial blooms mitigation by dredging is not well clarified. In eutrophic water remediation by dredging, shifts in interconnection between the bacterioplankton community and sediment biogeochemistry have rarely been investigated.

Based on the development of high-throughput sequencing and bioinformatics, knowledge of the composition and diversity of microbial communities in bloom-influenced water bodies is gradually expanding. However, these studies mainly report the effects of nutrient changes only on the diversity and composition of microbial communities. Few relevant studies have focused on the function and interaction of the bacterioplankton community in freshwater ecosystems with cyanobacterial blooms. In this study, we aimed to explore the mechanisms of how dredging could mitigate cyanobacterial blooms. We hypothesize that 1) dredging can significantly change water physicochemical properties and sediment biogeochemistry; 2) dredging can clearly decrease the abundance of bacterioplankton and cyanobacteria as well as the algae content; 3) dredging can significantly alter the diversity, composition, function, and interaction of bacterioplankton communities.