Flavobacterial exudates disrupt cell cycle progression and metabolism of the diatom Thalassiosira pseudonana

Abstract

Phytoplankton and bacteria form the base of marine ecosystems and their interactions drive global biogeochemical cycles. The effects of bacteria and bacteria-produced compounds on diatoms range from synergistic to pathogenic and can affect the physiology and transcriptional patterns of the interacting diatom. Here, we investigate physiological and transcriptional changes in the marine diatom Thalassiosira pseudonana induced by extracellular metabolites of a known antagonistic bacterium Croceibacter atlanticus. Mono-cultures of C. atlanticus released compounds that inhibited diatom cell division and elicited a distinctive morphology of enlarged cells with increased chloroplast content and enlarged nuclei, similar to what was previously observed when the diatom was co-cultured with live bacteria. The extracellular C. atlanticus metabolites induced transcriptional changes in diatom pathways that include recognition and signaling pathways, cell cycle regulation, carbohydrate and amino acid production, as well as cell wall stability. Phenotypic analysis showed a disruption in the diatom cell cycle progression and an increase in both intra- and extracellular carbohydrates in diatom cultures after bacterial exudate treatment. The transcriptional changes and corresponding phenotypes suggest that extracellular bacterial metabolites, produced independently of direct bacterial-diatom interaction, may modulate diatom metabolism in ways that support bacterial growth.

Impact of airborne algicidal bacteria on marine phytoplankton blooms

“…Recently, there have been documented isolations of pathogenic bacteria that can infect other phytoplankton groups such as diatoms [ 34 , 35 ]. Therefore, the aerial infection mechanism of bacterial pathogens may have a broad implication to diverse algal–bacteria interactions.…”

Microbial community composition and metabolic potential during a succession of algal blooms from Skeletonema sp. to Phaeocystis sp.

“…Even so, Flavobacteriaceae and Phaeocystis may have a mutually beneficial symbiotic relationship because Flavobacteriaceae maintained a higher abundance in the pre-stage of Phaeocystis bloom ( Figures 4B , 7 ). Recent evidence documented that Flavobacterial exudates can change the morphology of algal cells, which causes algal cells to become larger and secrete more carbohydrates ( Bartolek et al, 2022 ). Current phylogenetic analyses of the marine microbiome by experimental and natural phytoplankton blooms suggest that members of Flavobacteriaceae (i.e., Polaribacter , Robiginitalea ) are commonly associated with the bloom development of the Phaeocystis population ( Wemheuer et al, 2015 ; Li et al, 2020 ).…”

Cryptic bacterial pathogens of diatoms peak during senescence of a winter diatom bloom

“…Laboratory study demonstrated that C. atlanticus directly attaches to diatoms and inhibits cell division. Moreover, C. atlanticus exudates caused increases in intra-and extracellular carbon in Thalassiosira pseudonana, suggesting that bacterial antagonists can modulate host metabolism to support their growth (Bartolek et al, 2022).…”