Benthic cyanobacterial detritus mats in lacustrine sediment: Characterization and odorant producing potential

Highlights

• Multiple descriptive parameters were measured to identify phytodetritus mats.

• Phytodetritus mats were characterized as anoxic, reductive and low pH.

• Odorants were associated with biodegradable compounds in the phytodetritus mats.

• Phytodetritus mats are an overlooked source of odorants in the sediment.

Abstract

Eutrophic freshwater lake ecosystems are receiving increasing public attention due to a global increase in large-scale harmful cyanobacterial blooms in surface waters. However, the contribution of phytodetritus accumulation in benthic sediments post-bloom remains unclear. In this study, field investigations were performed using microsensors to evaluate benthic phytodetritus mats by measuring TOC/TN ratios, pigments, biodegradable compounds and odorants as descriptive parameters. Results show that the massive amount of phytodetritus trapped by aquatic plants gradually evolved into benthic cyanobacterial detritus mats, which were characterized as anoxic, reductive and low pH. It was confirmed that the occurrence of odorants is more serious in the detritus mats due to decay and decomposition of the accumulated phytodetritus. The mean odorant content in the vegetated zones was 3–52 times higher than that in the unvegetated zones. The dominant odorants were dimethyl trisulfide (DMTS), β-ionone and β-cyclocitral, with mean contents of 52.38 ng·(g·dw)-1, 162.20 ng·(g·dw)-1 and 307.51 ng·(g·dw)-1, respectively, in the sediment. In addition, odorant production appears to be associated with the distribution of biodegradable compounds in the sediment. This is supported by the marked correlation observed between biodegradable compounds and odorants. Multiple regression analysis showed that biodegradable compounds can be used as indicators to predict odorant content in the sediment. It is noteworthy that the odorant trend in the water column and sediment is symmetrical, indicating a risk of diffusion from the sediment to the water column. This study helps to clarifying the contributions of benthic cyanobacterial detritus mats to odorant production in shallow eutrophic lakes. The information provided herein may also be useful for future management of aquatic ecosystems.

Introduction

Cyanobacterial blooms are occurring globally at an increasing frequency, magnitude and duration (Michalak et al., 2013; Paerl and Huisman, 2008; Worden and Wilken, 2016; Zhang et al., 2018). A close coupling of this phenomenon to rapid sedimentation of cyanobacterial detritus in the benthic ecosystem has caused increasing concern (Braeckman et al., 2019; Woszczyk et al., 2011; Yu et al., 2013; Zhang et al., 2010). As this high level of phytodetritus accumulation rapidly occurs, it results in negative effects on the sediment system, such as deoxygenation, toxin production, offensive odorants and potential risk to drinking water supplies (Wang et al., 2019; Watson et al., 2016; Xu et al., 2015). Previous studies have primarily focused on the decay and decomposition processes of thick harmful cyanobacterial blooms on surface water (Guo et al., 2019; Yu et al., 2016; Zhang et al., 2016), whereas the massive aggregate of cyanobacterial detritus in sediments after the collapse of the blooms has been neglected even though it has far-reaching consequences on freshwater lake ecosystems (Su et al., 2019). Therefore, it is imperative to evaluate the composition and fate of the benthic cyanobacterial detritus mats and the associated effects on aquatic ecosystems.

The formation of cyanobacterial detritus mats is favored by a high level of cyanobacterial blooms, a high sedimentation rate and a high density of aquatic plants (Cai et al., 2017; Qi et al., 2019b; Su et al., 2019). In large and shallow lakes, massive cyanobacterial blooms are generally driven by the wind, resulting in accumulation in the littoral zone or entrapment in macrophytes (Liu et al., 2017; Xing et al., 2011). In vegetated littoral zones, the cyanobacterial biomass can be 3000 to 4500 times higher than that in the unvegetated zones (Wang et al., 2006). Following accelerated growth, cell death and bloom lysis results in a net accumulation of cyanobacterial detritus on the sediment surface, forming a dense benthic bioclastic mat (Xing et al., 2011). Previous studies show the presence of cyanobacterial detritus at up to 70 cm below the sedimentary interface (Latour et al., 2007). According to earlier descriptions, benthic phytodetritus may have three fates (Braeckman et al., 2019; Yu et al., 2013; Zhang et al., 2010). Firstly, it could be partially assimilated into new biomass, acting as an important food source for bivalves, shrimp and amphipods (Ramirez-Llodra et al., 2016; Renaud et al., 2015). Secondly, a larger fraction of the detritus may decay and decompose, or be released as dissolved organic matter, returning to the water column (Yu et al., 2013). Thirdly, phytodetritus, which also contains refractory material, can be buried below the sediment surface, thereby locking it away from exchange with the overlying water (Otten et al., 1992). When cyanobacterial detritus sedimentation occurs rapidly and in large amounts after the collapse of the bloom, the sediment system is unable to cope. The imbalance between microbial degradation and continuous input could cause a serious ecosystem disaster (Huang et al., 2018; Xu et al., 2015).

In addition, the abundance and composition of cyanobacteria-derived bioclastic accumulation in lake sediments varies considerably with local conditions, exerting different effects on the biogeochemical processes in lake ecosystems (García-Robledo et al., 2008; Zhang et al., 2017). Firstly, the aggregation and decomposition of cyanobacterial detritus can potentially change the biological and physical characteristics of the benthic environment, such as the dissolved oxygen (DO), redox state (Eh) and pH of the water-sediment profiles, which can significantly affect nutrient cycling (Deng et al., 2019; Han et al., 2015). Secondly, because cyanobacterial detritus contains a large amount of nutrients, such as carbon and nitrogen (Zhu et al., 2013), it serves as a mobile nutrient reservoir. Burial and decomposition of massive cyanobacterial detritus can fuel carbon and nitrogen sedimentation, which may in turn spur cyanobacterial blooms that can either be promptly mineralized or assimilated to enter the food web (Rossi, 2007). Thirdly, massive sedimentary cyanobacterial detritus in static and highly eutrophic water bodies, in combination with excessive nutrient loading, may result in black water blooms (Duan et al., 2014; He et al., 2018; Zhou et al., 2015) that are associated with the release of a large amount of odorants, including dimethyl sulfide (DMS), dimethyl disulfide (DMDS), dimethyl trisulfide (DMTS), 2-methylisoborneol (2-MIB), geosmin, β-ionone and β-cyclocitral (Harris and Graham, 2017; Shang et al., 2018; Wang et al., 2019).

These events present a marked risk to aquatic ecosystems and have been observed in Lake Greifensee, Lake Zurich, Lake Lucerne, Lake Chaohu and Lake Taihu (Deng et al., 2019; Paerl and Huisman, 2010; Yan et al., 2015). As such, the decay and decomposition processes of cyanobacterial blooms in the water column have been extensively studied (Chen et al., 2010; Guo et al., 2019; Lee et al., 2017; Zhang et al., 2016). However, the composition and fate of sedimentary detritus resulting from large-scale cyanobacterial blooms, as well as the possible links with offensive odorants in benthic ecosystems, remain unclear.

Hence, this study sought to understand the composition and fate of the increasing amount of cyanobacterial detritus in benthic ecosystems, as well as the associated odorant production in the sediment. Specifically, benthic phytodetritus derived from cyanobacteria, a dominant phytoplankton species of the eutrophic Lake Taihu ecosystem was investigated. Vertical microprofiles were obtained for DO, H₂S, Eh and pH at the sediment-water interface, and the sedimentary total nitrogen (TN) and total organic carbon (TOC) contents were measured. In addition, the vertical distribution of pigments, biodegradable compounds and odorants in the vegetated and unvegetated zones were compared. Finally, the relationship between odorants and biodegradable compounds was clarified by multiple regression analysis and the likely source of odorants in the water column was proposed. These results could be helpful for clarifying the contributions of benthic cyanobacterial detritus decomposition to odorant production in shallow eutrophic lakes and may also be useful for future management of aquatic ecosystems.