Contrasting Mechanisms Determine the Microeukaryotic and Syndiniales Community Assembly in a Eutrophic bay.

Syndiniales is a diverse parasitic group, increasingly gaining attention owing to its high taxonomic diversity in marine ecosystems and inhibitory effects on the dinoflagellate blooms. However, their seasonal dynamics, host interactions, and mechanisms of community assembly are largely unknown, particularly in eutrophic waters. Here, using 18S rRNA gene amplicon sequencing, we intended to elucidate the interactions between Syndiniales and microeukaryotes, as well as community assembly processes in a eutrophic bay. The results showed that Syndiniales group II was dominating throughout the year, with substantially higher abundance in the winter and spring, whereas Syndiniales group I was more abundant in the summer and autumn. Temperature and Dinoflagellata were the most important abiotic and biotic factors driving variations of the Syndiniales community, respectively. The assembly processes of microeukaryotes and Syndiniales were completely different, with the former being controlled by a balance between homogeneous selection and drift and the latter being solely governed by drift. Network analysis revealed that Syndiniales group II had the largest number of interactions with microeukaryotes, and they primarily associated with Dinoflagellata in the winter, while interactions with Chlorophyta and Bacillariophyta increased dramatically in summer and autumn. These findings provide significant insights in understanding the interactions and assembly processes of Syndiniales throughout the year, which is critical in revealing the roles of single-celled parasites in driving protist dynamics in eutrophic waters.

Interaction patterns and assembly mechanisms of dinoflagellates and diatoms in a coastal bay suffering from long-term eutrophication.

Dinoflagellates and diatoms are highly prevalent and ecologically important phytoplankton in coastal waters, greatly contributing to primary productivity in marine ecosystems. Although their composition and diversity have been extensively elucidated in the open ocean, their interaction patterns and community assembly in long-term eutrophic coastal waters remain poorly understood. This investigation aimed to elucidate the seasonal successional patterns of dinoflagellates and diatoms by 18S rRNA gene amplicon sequencing in a semi-enclosed bay. The results revealed that dinoflagellate and diatom communities have pronounced seasonal succession patterns, which are primarily associated with temperature. Furthermore, the most prevalent species throughout the year were Heterocapsa rotundata and Skeletonema costatum. Moreover, the assembly of dinoflagellate and diatom communities was mainly dominated by stochastic processes, with drift being the major factor. The co-occurrence of dinoflagellates and diatoms showed seasonal patterns, with the highest interactions observed in autumn. In addition, interactions of Syndiniales with dinoflagellates and diatoms highlighted the roles of parasites in eutrophic conditions. Flavobacteriaceae and Rhodobacteraceae are the bacterial taxa that most frequently interacted with dinoflagellates and diatoms, with interactions between dinoflagellates and bacteria being more complex than those between diatoms and bacteria. Overall, this study provides results that deepen our understanding of the phytoplankton dynamics in coastal eutrophic waters.IMPORTANCEDinoflagellates and diatoms are major phytoplankton groups in coastal waters. The composition and diversity of dinoflagellates and diatoms in the open ocean have been well documented; however, it remains uncertain to what extent their adaptation to long-term eutrophic conditions influences their response to environmental disturbances. Here, we investigated the interactions and assembly processes of dinoflagellates and diatoms in a eutrophic bay throughout the whole year. Our findings revealed that interactions between dinoflagellates and diatoms are primarily shaped by seasonal transitions, while prolonged eutrophic conditions tend to amplify stochastic processes in community assembly. These findings provide novel perspectives on the influence of long-term eutrophication on phytoplankton dynamics within eutrophic waters.

Elevated temperature alters bacterial community from mutualism to antagonism with Skeletonema costatum: insights into the role of a novel species, Tamlana sp. MS1.

Skeletonema costatum, a cosmopolitan diatom primarily inhabiting coastal ecosystems, exhibits a typically close yet variable relationship with heterotrophic bacteria. The increasing temperature of surface seawater is expected to substantially affect the viability and ecological dynamics of S. costatum, potentially altering its relationship with bacteria. However, it remains unclear to what extent the elevated temperature could change these relationships. Here, the relationship between axenic S. costatum and natural seawater bacteria underwent a dramatic shift from mutualism to antagonism as the co-culture temperature increased from 20°C to 25°C. The co-occurrence network indicated significantly increased complexity of interaction between S. costatum and bacteria community after temperature elevation, especially with Flavobacteriaceae, implying their potential role in eliminating S. costatum under higher temperatures. Additionally, a Flavobacteriaceae isolate, namely MS1 identified as Tamlana genus, was isolated from the co-culture system at 25°C. MS1 had a remarkable ability to eliminate S. costatum, with the mortality rate at 25°C steadily rising from 30.2% at 48 h to 92.4% at 120 h. However, it promoted algal growth to some extent at 20°C. These results demonstrated that increased temperature promotes MS1 shifts from mutualism to antagonism with S. costatum. According to the comparative genomics analysis, changes in the lifestyle of MS1 were attributed to the increased gliding motility and attachment of MS1 under elevated temperature, enabling it to exert an algicidal effect through direct contact with alga. This investigation provided an advanced understanding of interactions between phytoplankton and bacteria in future warming oceanic ecosystems. IMPORTANCE: Ocean warming profoundly influences the growth and metabolism of phytoplankton and bacteria, thereby significantly reshaping their interactions. Previous studies have shown that warming can change bacterial lifestyle from mutualism to antagonism with phytoplankton, but the underlying mechanism remains unclear. In this study, we found that high temperature promotes Tamlana sp. MS1 adhesion to Skeletonema costatum, leading to algal lysis through direct contact, demonstrating a transition in lifestyle from mutualism to antagonism with increasing temperature. Furthermore, the gliding motility of MS1 appears to be pivotal in mediating the transition of its lifestyle. These findings not only advance our understanding of the phytoplankton-bacteria relationship under ocean warming but also offer valuable insights for predicting the impact of warming on phytoplankton carbon sequestration.

Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay.

Eutrophication occurring in coastal bays is prominent in impacting local ecosystem structure and functioning. To understand how coastal bay ecosystem function responds to eutrophication, comprehending the ecological processes associated with microbial community assembly is critical. However, quantifying the contribution of ecological processes to the assembly of prokaryotic communities is still limited in eutrophic waters. Moreover, the influence of these ecological processes on microbial interactions is poorly understood. Here, we examined the assembly processes and co-occurrence patterns of prokaryotic communities in a eutrophic bay using 156 surface seawater samples collected over 12 months. The variation of prokaryotic community compositions (PCCs) could be mainly explained by environmental factors, of which temperature was the most important. Under high environmental heterogeneity conditions in low-temperature seasons, heterogeneous selection was the major assembly process, resulting in high ß-diversity and more tightly connected co-occurrence networks. When environmental heterogeneity decreased in high-temperature seasons, drift took over, leading to decline in ß-diversity and network associations. Microeukaryotes were found to be important biological factors affecting PCCs. Our results first disentangled the contribution of drift and microbial interactions to the large unexplained variation of prokaryotic communities in eutrophic waters. Furthermore, a new conceptual model linking microbial interactions to ecological processes was proposed under different environmental heterogeneity. Overall, our study sheds new light on the relationship between assembly processes and co-occurrence of prokaryotic communities in eutrophic waters. IMPORTANCE A growing number of studies have examined roles of microbial community assembly in modulating community composition. However, the relationships between community assembly and microbial interactions are not fully understood and rarely tested, especially in eutrophic waters. In this study, we built a conceptual model that links seasonal microbial interactions to ecological processes, which has not been reported before. The model showed that heterogeneous selection plays an important role in driving community assembly during low-temperature seasons, resulting in higher ß-diversity and more tightly connected networks. In contrast, drift became a dominant force during high-temperature seasons, leading to declines in the ß-diversity and network associations. This model could function as a new framework to predict how prokaryotic communities respond to intensified eutrophication induced by climate change in coastal environment.