The formation and dissipation of algal blooms, which are caused by the rapid growth of one or more phytoplankton species, are known to be affected by various environmental factors, such as temperature, salinity, eutrophic conditions, and light intensity (Higashi et al., 2016). The interactions between algae and other organisms, such as marine bacteria that rely on the organic matter secreted by algae, are crucial for algal growth (Anderson et al., 2002; Higashi et al., 2016). The community compositions of bacteria, which play critical roles in the marine ecosystem by participating in biochemical reactions and associate with chemical transformations of almost all elements, are sensitive to environmental changes (Arrigo, 2004; Comte and Del Giorgio, 2010; Ruiz-Gonzalez et al., 2013; Sun et al., 2017; Xia et al., 2020). Previous studies have suggested that bacterial communities can be significantly influenced by algal blooms, such as diatom blooms (Liu et al., 2019; Sun et al., 2020), dinoflagellate Karenia brevis blooms (Meyer et al., 2014), and dinoflagellate Noctiluca scintillans blooms in marine waters (Xia et al., 2020). Therefore, it is hypothesized that the occurrence of Phaeocystis globosa bloom in this study is likely to have a substantial impact on bacteria.

A wide range of interactions between bacteria and phytoplankton determine the composition of bacterial communities (Cole, 1982; Sher et al., 2011; Delmont et al., 2014). Most marine bacteria in seawater are free-living (bacterioplankton), while some are attached bacteria with sophisticated interactions with their hosts (Worden et al., 2015). Bacteria can decompose organic matter such as microalgae cells and use algal polysaccharides as a carbon source (Teeling et al., 2016), making attached bacteria more important in the dissipation of bloom due to their interaction with their attached host. However, most research has focused on bacterioplankton and its interaction with algae, neglecting information on community structures of attached bacteria and their temporal variations with bloom development, which is essential for understanding the complex interactions between microalgae and bacteria, quite limited (Meyer et al., 2014; Li et al., 2020).

In January 2021, a bloom of P. globosa, which alternates between solitary cells (3–10 μm in diameter) and gelatinous colonies (3 cm in maximal diameter), occurred for the first time in Mirs Bay, southern China (Wang et al., 2021a; Wang et al., 2021b). Of the seven identified colony-forming Phaeocystis species, P. globosa is the most widespread, and its bloom could affect the bacterioplankton community by environmental filtering of specific taxa (Li et al., 2020). The gelatinous colonies of P. globosa may also favor the attachment of specific bacteria, further affecting the blooming process. To understand the effects of P. globosa bloom, it is necessary to consider not only bacterioplankton but also attached bacteria, may play an important role in the outbreak and dissipation of algal blooms.

In this study, we investigated the community profiles of bacteria during a P. globosa bloom in Mirs Bay, southern China. Bacteria living in three habitats, i.e., bacterioplankton, particle-attached bacteria, and colony-attached bacteria, were studied from the exponential growth phase to the decline growth phase of the bloom. This study aimed to investigate the differences in bacterial communities among three habitats and their temporal variations during blooming, as well as the interactions between microalgae and bacteria.

The bacterial communities harbored in the three habitats were influenced by the inhabited niches and the growth phases of microalgae bloom. We found marked variations in bacterial community structures among the three types of bacteria, potentially due to the diverse lifestyles of bacterioplankton and attached bacteria (Acinas et al., 1999; Fuchsman et al., 2011; Li et al., 2015). The physical and biochemical characteristics of bacterial hosts impact their diversity, with particle-attached bacteria exhibiting greater diversity than bacterioplankton and colony-attached bacteria, consistent with the findings in the Black and Beaufort Seas (Fuchsman et al., 2011; Ortega-Retuerta et al., 2013). In contrast, a lower taxonomic richness of particle-attached bacterial communities compared with bacterioplankton was reported by Li et al. (2015) in the South China Sea, which may be attributed to the P. globosa bloom outbreak in the present study. Further research is required to gain a better understanding of the mechanisms involved.

The present study showed that the characteristics of bacterial communities were related to the growth phases of microalgae bloom, likely due to the varying availability of substrates. Exopolysaccharides were the most available polysaccharides at the beginning of the bloom and were utilized first by most bacteria species. As the bloom progressed, recalcitrant substrates such as sulfated polysaccharides in cellular substrates become dominant, allowing specific bacteria to acquire a dominant position (Teeling et al., 2016). These differences in substrate availabilities at different growth phases of P. globosa bloom likely caused the variations in dominant species and the richness of bacterial communities. Additionally, the change of bloom species also influenced the bacterial community. The A. sanguinea bloom at station S2 on January 28 caused a marked shift in the bacterial communities of bacterioplankton and particle-attached bacteria ( Figure S1 ). For example, Candidatus puniceispirillum, a member of the SAR11 clade of Alphaproteobacteria, increased significantly compared to station S1 on January 28 and station S2 on January 26. C. pelagibacter, another member of the SAR11 clade, is known to be a dominant genus in the bacterial community and plays a crucial role in carbon cycling during A. sanguinea blooms (Yang et al., 2012). Therefore, the explosive growth of C. puniceispirillum during the A. sanguinea bloom in this study may be attributed to their similar abilities to C. pelagibacter.

It has been reported that the dominant phyla of bacterioplankton in the South China Sea are Proteobacteria and Cyanobacteria (Shi et al., 2018; Sun et al., 2021; Ren et al., 2022). However, the present study found that Bacteroidota was the most abundant bacterioplankton, likely due to the high concentrations of nutrients (e.g. PO 4 3 − ) that favor these organisms during bloom periods, as well as their ability to degrade complex proteins and mucopolysaccharides released by P. globosa (Cottrell and Kirchman, 2000; Janse et al., 2000; Brussaard et al., 2005; Lamy et al., 2009; Almutairi, 2015). Remarkable differences in bacterial community structure and diversity were also observed between the exponential and decline growth phases of the bloom, likely due to the increased proportion of recalcitrant polysaccharides (e.g., fucose-containing sulfated polysaccharides) derived from algal fragmentation, which favored specific bacteria such as Persicirhabdus sp. of Verrucomicrobiota (Martinez-Garcia et al., 2012; Sichert et al., 2020; Orellana et al., 2021). On the other hand, the dominant bacterioplankton that differed significantly between the exponential and the decline growth phases of bloom were all belonged to Bacteroidota, indicating their important role in the degradation of complex organic carbon, particularly in the forms of polysaccharides and hydrocarbons (Bauer et al., 2006; Wolińska et al., 2017). The amounts of organic matter which served as electron donors for organic matter-degrading bacteria such as denitrifying bacteria and sulfate-reducing bacteria can be evaluated by the COD value. In the present study, the community structures of bacterioplankton were positively correlated with COD during the exponential growth phase of the bloom. Notably, the COD value decreased drastically as the bloom developed into the decline phase due to algal cell death or sinking to the bottom, yet the bacterioplankton community did not change accordingly that much. This suggested that the bacterioplankton community was regulated not only by the quantity of organic matter but also by its quality, i.e., biological and chemical composition and form characteristics (Stelzer et al., 2014). Furthermore, environmental factors such as temperature, salinity, and pH were also essential in shaping the community profiles of bacterioplankton.

Particle-attached bacteria possess a critical capability of attaching to particulate matters including Phaeocystis aggregates, providing them many advantages including increased nutrient acquisition, reduced predation risk, and enhanced interactions among populations (Dang et al., 2008). The aggregates of particles or microalgae cells serve as organic-rich microhabitats with abundant substrates, harboring large amounts of bacteria (Alldredge et al., 1986; Li et al., 2015). In the present study, Proteobacteria (Alphaproteobacteria and Gammaproteobacteria) was the dominant phylum of particle-attached bacteria due to their great adhesion ability, as reported by Li et al. (2015). As the bloom shifted from the exponential phase to the decline phase, the homogeneity of their hosts (dominated by algal fragments) caused a significant decrease in the community diversity of particle-attached bacteria (Kiørboe and Jackson, 2001; Azam and Malfatti, 2007; Fang et al., 2015). In addition, the dissolved organic matter released into ambient waters was further utilized by bacterioplankton, such as Persicirhabdus sp. of Verrucomicrobiota, whose abundance significantly increased in the decline growth phase of the bloom, resulting in the complex relationship among organic particles, phytoplankton, particle-attached bacteria, and bacterioplankton, and further studies are needed to explore this.

The formation and enlargement of gelatinous colony is a defense strategy for Phaeocystis, allowing them to avoid predation and become cosmopolitan marine phytoplankton (Wang et al., 2015; Wang et al., 2021a). These colonies are capable of maintaining their position in the euphotic zone by regulating their buoyancy based on light intensity and water flow (Wang et al., 2010). Correspondingly, the majority of colony-attached bacteria were species belonging to autotrophic cyanobacteria, which require light absorption for photosynthesis. Intensive host selection pressure (unique host) resulted in the lowest diversity of colony-attached bacteria, but this could also be an advantage in maintaining the stability of symbiotic relationships between colony-associated bacteria and their hosts (Edwards et al., 2015). A more complex microbial ecosystem with greater connectivity is more stable and robust during environmental changes, as indicated by the high network density, average degree, and the number of edges with the least nodes in colony-attached bacteria (Santolini and Barabási, 2018; Huang et al., 2022). This complex network may explain why there was no significant difference in colony-attached bacterial communities between the exponential and decline growth phases of the P. globosa bloom.

Our study reveals the profound impacts of P. globosa bloom on marine bacteria, with the bacterioplankton and particle-attached bacterial communities varying as the bloom progressed. Bacteria, particularly those with organic decomposing abilities (e.g., Verrucomicrobiota and Bacteroidota), could play a key role in the dissipation of P. globosa blooms. Our findings emphasize the importance of studying the intricate connections between bacteria and microalgae blooms.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/genbank/, PRJNA776989.

RS and HH conceived the original ideas and collected samples during the outbreak of P. globosa bloom for the manuscript. RS developed the outline and analyzed the data, prepared the manuscript with some contributions to drafting from SZ, MD, and TH and critical refinement by ZQ. All authors contributed to the article and approved the submitted version.