Phycosphere Microbial Succession Patterns and Assembly Mechanisms in a Marine Dinoflagellate Bloom

Abstract

Given the ecological significance of microorganisms in algal blooming events, it is critical to understand the mechanisms regarding their distribution under different conditions. We tested the hypothesis that microbial community succession is strongly associated with algal bloom stages, and that the assembly mechanisms are cocontrolled by deterministic and stochastic processes. Community structures and underlying ecological processes of microbial populations (attached and free-living bacteria) at three algal bloom stages (pre-, during, and postbloom) over a complete dinoflagellate Scrippsiella trochoidea bloom were investigated. Both attached and free-living taxa had a strong response to the bloom event, and the latter was more sensitive than the former. The contribution of environmental parameters to microbial variability was 40.2%. Interaction analysis showed that complex positive or negative correlation networks exist in phycosphere microbes. These relationships were the potential drivers of mutualist and competitive interactions that impacted bacterial succession. Null model analysis showed that the attached bacterial community primarily exhibited deterministic processes at pre- and during-bloom stages, while dispersal-related processes contributed to a greater extent at the postbloom stage. In the free-living bacterial community, homogeneous selection and dispersal limitation dominated in the initial phase, which gave way to more deterministic processes at the two later stages. Relative contribution analyses further demonstrated that the community turnover of attached bacteria was mainly driven by environmental selection, while stochastic factors had partial effects on the assembly of free-living bacteria. Taken together, these data demonstrated that a robust link exists between bacterioplankton community structure and bloom progression, and phycosphere microbial succession trajectories are cogoverned by both deterministic and random processes. IMPORTANCE Disentangling the mechanisms shaping bacterioplankton communities during a marine ecological event is a core concern for ecologists. Harmful algal bloom (HAB) is a typical ecological disaster, and its formation is significantly influenced by alga-bacterium interactions. Microbial community shifts during the HAB process are relatively well known. However, the assembly processes of microbial communities in an HAB are not fully understood, especially the relative influences of deterministic and stochastic processes. We therefore analyzed the relative contributions of deterministic and stochastic processes during an HAB event. Both free-living and attached bacterial groups had a dramatic response to the HAB, and the relative importance of determinism versus stochasticity varied between the two bacterial groups at various bloom stages. Environmental factors and biotic interactions were the main drivers impacting the microbial shift process. Our results strengthen the understanding of the ecological mechanisms controlling microbial community patterns during the HAB process.

Cyanobacterial blooms contribute to the diversity of antibiotic-resistance genes in aquatic ecosystems

“…Interestingly, our results suggested that aquatic bacteria and Planktothrix could be symbiotic mutualists, which may increase the probability of ARBs. Cyanobacteria typically release various low-molecular-weight molecules during blooms, including glucose, organic acids, amino acids and sugar alcohols, which may benefit phycospheric bacteria 7 , 52 . One study has demonstrated that Planktothrix could resist parasitic fungi by secreting hassallidin, an antifungal peptide 53 .…”

“…According to the morphology of Planktothrix and Microcystis under scanning electron microscopy, this filamentous cyanobacterium can provide a larger habitat for the survival of bacteria, which is termed as the “cyanosphere” 7 : the region in the immediate vicinity of cyanobacteria containing rich cyanobacterial secretions. Moreover, compared with other filamentous cyanobacteria, Planktothrix has a stronger carbon and nitrogen metabolism capacity for the use of surrounding bacteria 57 .…”

“…Such blooms are increasingly frequent in freshwater and marine environments; 30-40% of the world's lakes and reservoirs and nearly 80% of the freshwater bodies in China are eutrophic 2 . Cyanobacterial blooms decrease water quality and adversely affect the functioning of aquatic ecosystems [3][4][5][6][7] , which can alter the bacterial community structure and disrupt recreation and human health 8,9 . Unique microbial communities are assembled during a cyanobacterial bloom by stochastic and potentially deterministic processes, including competition, mutualism, and trade-offs 10 .…”

Core bacteria associated with Cochlodinium polykrikoides(Dinophyta) blooms: diversity and function

“…Interactions between phytoplankton and bacteria play significant roles in shaping biogeochemical cycles (Azam & Malfatti, 2007). This interconnection and co-influence between bacteria and phytoplankton (particularly the strong responses of HABs) is known as the phycosphere (Zhou et al, 2019). The marine phycosphere of specific bacteria and phytoplankton has precise cross-associations for the stimulation and inhibition of both groups (Sapp et al, 2007).…”

“…Although some recent reports have suggested that specific bacteria are associated with HABs (Jung et al, 2021;Kang et al, 2021), ecological studies on these interactions are lacking. Moreover, the ecological interaction and function between bacteria and phytoplankton can be difficult to explain fully, because the phycosphere habitat may determine how communities are organised; for example, it can provide ecological niches where species interactions, such as competition, mutualism, and predation, occur, in addition to providing a suitable environment (Sapp et al, 2007;Zhou et al, 2019).…”