Metaproteomics reveals major microbial players and their metabolic activities during the blooming period of a marine dinoflagellateProrocentrum donghaiense

Abstract

Interactions between bacteria and phytoplankton during bloom events are essential for both partners, which impacts their physiology, alters ambient chemistry and shapes ecosystem diversity. Here, we investigated the community structure and metabolic activities of free-living bacterioplankton in different blooming phases of a dinoflagellate Prorocentrum donghaiense using a metaproteomic approach. The Fibrobacteres-Chlorobi-Bacteroidetes group, Rhodobacteraceae, SAR11 and SAR86 clades contributed largely to the bacterial community in the middle-blooming phase while the Pseudoalteromonadaceae exclusively dominated in the late-blooming phase. Transporters and membrane proteins, especially TonB-dependent receptors were highly abundant in both blooming phases. Proteins involved in carbon metabolism, energy metabolism and stress response were frequently detected in the middle-blooming phase while proteins participating in proteolysis and central carbon metabolism were abundant in the late-blooming phase. Beta-glucosidase with putative algicidal capability was identified from the Pseudoalteromonadaceae only in the late-blooming phase, suggesting an active role of this group in lysing P. donghaiense cells. Our results indicated that diverse substrate utilization strategies and different capabilities for environmental adaptation among bacteria shaped their distinct niches in different bloom phases, and certain bacterial species from the Pseudoalteromonadaceae might be crucial for the termination of a dinoflagellate bloom.

Diatoms shape the biogeography of heterotrophic prokaryotes in early spring in the Southern Ocean

“…Similarly, Rhodobacterales had a higher number of strong positive correlations with Thalassionema nitzschoides and Chaetoceros curvisetus than with Fragilariopsis kerguelensis. The rapid response of the above mentioned OTUs to phytoplankton blooms has been attributed to their uptake capacities of specific phytoplankton-derived substrates, using functional profiling based on metatranscriptomics (Rinta-Kanto et al, 2012;Teeling et al, 2012;Beier et al, 2015) and metaproteomics (Li et al, 2018). We expected the composition of total and active prokaryotes to be different, but the spatial distribution and the co-occurrence patterns revealed to be highly similar between these communities.…”

“…Noticeably strong correlations were also found for deltaproteobacterial SAR324 OTUs. The rapid response of the above mentioned OTUs to phytoplankton blooms has been attributed to their uptake capacities of specific phytoplankton-derived substrates, using functional profiling based on metatranscriptomics (Rinta-Kanto et al, 2012;Teeling et al, 2012;Beier et al, 2015) and metaproteomics (Li et al, 2018). In contrast, Thalassionema nitzschoides and Chaetoceros curvisetus had strong correlations with OTUs that were previously identified as rapid responders to phytoplankton blooms, as for example the flavobacterial OTUs Polaribacter, Ulvibacter and OTUs from the NS7 group (Buchan et al, 2014).…”

“…Phytoplankton blooms markedly affect the prokaryotic community composition (see reviews by Buchan et al, 2014;Bunse and Pinhassi, 2017). The successional shifts were linked to the temporal modifications in the quantity and quality of the phytoplankton-derived DOM providing new niches for either opportunistic prokaryotic taxa or those adapted in the preferential utilization of the compounds released (Rinta-Kanto et al, 2012;Sarmento and Gasol, 2012;Teeling et al, 2012;Li et al, 2018). Using the exudate of a common diatom species as a growth substrate in an experimental approach and in situ observations allowed to establish a link between substrate preferences of several prokaryotic taxa and their presence during spring phytoplankton blooms in the Southern Ocean (Landa et al, 2016).…”

Metatranscriptomic Signatures Associated With Phytoplankton Regime Shift From Diatom Dominance to a Dinoflagellate Bloom

“…Temperature, salinity, and turbidity were measured using CTD (SBE 17plus V2, Sea-Bird Scientific, United States) at each sampling event. Concentrations of dissolved inorganic nitrogen (DIN) (ammonium, nitrate, and nitrite), silicate and phosphate were determined using continuous flow analyzer, all measurements were performed on triplicate samples San ++ (SKALAR, Breda, Holland) (Li et al, 2017).…”

Mesozooplankton taurine production and prokaryotic uptake in the northern Adriatic Sea

“…Dissolved organic matter (DOM) released by crustacean zooplankton and phytoplankton can generate shifts in the prokaryotic community composition on a time scale of a few hours to days (Valdés et al 2017; Choi et al 2018). Members of SAR11 and Rhodobacteraceae are often present in high abundances during bloom events (Alonso and Pernthaler 2006; Choi et al 2018), utilizing taurine and other low‐molecular weight organic compounds (Li et al 2018). Toward the decline of a bloom, however, other prokaryotic groups dominate the community, such as Bacteroidetes, degrading high‐molecular weight organic compounds (Alonso and Pernthaler 2006; Choi et al 2018).…”