Synechococcus bloom in the Pearl River Estuary and adjacent coastal area–With special focus on flooding during wet seasons

Highlights

• Small phytoplankton, especially Synechococcus and nanoeukaryotes, contribute to the blooms in the lower Pearl River Estuary.

• Phycocyanin-rich Synechococcus have wide salinity tolerances and occur in high abundance in the lower estuary.

• The two groups of phycoerythrin-rich Synechococcus have different salinity tolerances.

• Different niche segregation among picocyanobacterial clades can be identified from the OTUs of 16S rDNA.

• Synechococcus blooms show close interactions with active bacteria, particularly for Rhodobacteria and Actinobacteria.

Abstract

Based on the field surveys aimed at understanding the variations of Synechococcus (Syn) abundance in the Pearl River Estuary during different seasons. We found that heavy terrestrial precipitation result in significant riverine runoffs and promote Syn growth, extension and blooms during warm and wet seasons. To understand the ecological role of Syn play in this estuary during wet seasons, we combined flow cytometry and high throughput sequencing (HTS) of 16S rDNA to investigate the phytoplankton distribution patterns and the potential shaping mechanisms during a typical wet season. During the cruise, picophytoplankton, especially Syn, and Nano-eukaryotes contributed importantly to the total phytoplankton biomass of the estuary. Syn can be further divided into phycoerythrin (PE)-rich Syn and phycocyanin (PC)-rich Syn, with PC-rich Syn about 1.5 times higher than PE-rich Syn in abundance. Both PE-rich Syn (60.75 × 10³ cells ml⁻¹) and PC-rich Syn (604.05 × 10³ cells ml⁻¹) reach the highest abundance at the lower part of the estuary. Moreover, PE-rich Syn can be divided into two subgroups which showed different salinity preference, with PE1 distributed in the high salinity area (with salinity >25) while PE2 in the middle salinity area (with salinity 7–20). Our results from the 16S rDNA sequencing also indicated abundant diversity and different niche adaptation of Syn with the operational taxonomic units (OTUs) along the estuary. Besides, analysis also indicated a tight correlation between estuarine Syn and active heterotrophic bacteria, especially groups of Rhodobacteria and Actionobacteria.

Introduction

Picocyanobacteria are among the most important primary producers in the open ocean, while studies reported that they can also be the main contributors and even form super-dense and long-term bloom in coastal areas and riverine estuaries (Phlips et al., 1999; Murrell and Lores, 2004; Ahlgren et al., 2014). There are two constitutes in picocyanobacteria, namely Prochlorococcus (Pro) and Synechococcus (Syn). Pro prefer warm and oligotrophic offshore environments, while Syn have much wide ecological range all over the land and the ocean (Partensky et al., 1999). Similar to other cyanobacteria, Syn ecotypes display differences in their accessory pigments and phycobilisomes which make them adapted to different wavelengths of light (Camacho et al., 2000). Based on phycobilisome composition, two groups of Syn have been identified, one rich in phycoerythrin (PE) and the other in phycocyanin (PC). Red colored PE-rich Syn uses green light effectively, whereas blue-green colored PC-rich Syn absorbs red light effectively (Marsac and Houmard, 1988). The preference for different light makes niche segregation for turbidity of PC-rich Syn and PE-rich Syn. In addition to turbidity, salinity, nutrient, temperature and other environmental factors have also been revealed to have important roles in shaping the distribution patterns and dominance of different ecotypes of Syn (Cai et al., 2010; Rajaneesh and Mitbavkar, 2013).

With the rapid development of urbanization, the environmental problems of estuaries have become increasingly serious. Excess amount of nutrients with fresh flow inject into estuarine ecosystems and stimulate rapid growth of phytoplankton, especially large phytoplankton like dinoflagellate and diatoms (Tang et al., 2003; Qi et al., 2004b; Shen et al., 2012). Phytoplankton blooms can dramatically change ambient biogeochemical factors, such as exhaustion of oxygen, release toxins and other secondary metabolites into surrounding waters. At the same time, estuaries play important roles in supporting abundant biodiversity via providing nursery grounds for a variety of organisms, such as valuable fish species. Hence, blooms (especially dinoflagellates and diatoms) and their biological impacts associated with eutrophication in estuaries have caused widespread concern. However, compared with the large sized counterpart, few studies focused on small picophytoplankton distribution patterns, blooms, and strategies of different ecotypes responding to variations in estuarine environments (Qiu et al., 2010; Śliwińska-Wilczewska et al., 2018).

The Pearl River Estuary (PRE), which situated at the middle of Guangdong-Hong Kong-Macao Greater Bay Area, is one of the most important coastal fishing grounds of the South China Sea. While the estuary suffers from dramatic increasing of nutrient loadings (especially nitrogen) with the rapid industrial and agricultural development in the last decades, the strong river plume originates from the Pearl River, which is the 17th largest river in the world in terms of water discharge volume, and 80% of the discharge associated with large precipitation occurred during the wet season (Tan et al., 2004; Ye et al., 2017). Associated with the flood, primary production rising and harmful algal blooms always occur in this area during warm and wet seasons (Tang et al., 2003; Qi et al., 2004a; Shen et al., 2011; Shen et al., 2012). Phytoplankton bloom at the lower estuary has been reported as a seasonal phenomenon in wet seasons of PRE, and the bloom of phytoplankton will drive a series of harmful effects to the estuarine ecological dynamics and fishery sustainability (Qian et al.). Whereas little is known about the phytoplankton biomass size fractions, community structures, and the associated shaping mechanisms of the bloom, which always accounts for >1000 km². According to previous cruises conducted during wet seasons, extremely high abundance of Syn has always been spotted in the lower estuary. However, little is known about the contribution of Syn to the lower estuary bloom and why the lower estuary harbors such a high abundance. In addition, studies also indicated that the blooms of Syn appear to be far more disastrous for their resources and environmental state than even toxic dinoflagellate blooms. Moreover, Syn blooms display contagious features and show a tendency to become persistent in many coastal areas (Śliwińska-Wilczewska et al., 2018). Thus, issues of Syn bloom require more attention and interest from researchers.

In this paper, firstly we use preliminary results to study the seasonal variations of Syn and its relationship with flood in the estuary and then we choose a typical wet season to study the role that how large floodings play in altering the dynamics of phytoplankton and enhancing phytoplankton biomass especially the Syn in the lower estuary. Besides, we also measured the environmental variables, and associated heterotrophic bacteria (HBA) to study the potential biotic and abiotic drivers which shaping the Syn distribution pattern and bloom during wet seasons.