Project description:Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly understood that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during interactions with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. The interaction displays two distinct phases: first, there is a coexisting phase in which the alga grows exponentially and the bacterium grows as well. The interaction shifts to pathogenic when the virulence of Sulfitobacter D7 towards E. huxleyi is invoked upon exposure to high concentrations of algal dimethylsulfoniopropionate (DMSP), which occurs when the algae reach stationary growth or when DMSP is applied exogenously to algae in exponential growth. We aimed to unravel the response of Sulfitobacter D7 to the pathogenicity-inducing compound, DMSP, and to different algae-derived infochemicals that affect the lifestyle of the bacterium. We grew Sulfitobacter D7 in conditioned media (CM) derived from algal cultures at the different growth phases, exponential and stationary (Exp-CM and Stat-CM, respectively), in which DMSP concentration is low and high, respectively. This enabled us to separate between different phases of the interaction with E. huxleyi, i.e., Exp-CM representing the coexisting phase, and Stat-CM representing the pathogenic phase. An additional pathogenicity-inducing treatment was Exp-CM supplemented with 100 µM DMSP (herein Exp-CM+DMSP). This condition mimicked co-cultures to which we added DMSP exogenously and thus induced Sulfitobacter D7 pathogenicity, which lead to death of exponentially growing E. huxleyi. In order to identify bacterial genes that are specifically responsive to DMSP, and are not affected by other algae-derived factors, we grew Sulfitobacter D7 in defined minimal medium (MM), lacking algal metabolites, supplemented with 100 µM DMSP (herein MM+DMSP), and examined the transcriptional response. After 24 h of Sulfitobacter D7 growth in all 5 media, triplicates were taken for transcriptomic analysis. Altogether, this experimental design allowed to expand our understanding on the bacterial response to DMSP, algal infochemicals and which of these are essential for coexistence and pathogenicity.

Project description:Animal-algal photosymbioses are a unique group of symbiotic relationships in which animals harbor photosynthetic algae within their cells and tissues. Both marine and freshwater sponges host algal endosymbionts. In previous work, we demonstrated that freshwater sponges can acquire these endosymbionts horizontally through algal infection and that potentially conserved evolutionary pathways may lead to the establishment of the endosymbioses including those involved in endocytosis, ion transport, vesicle-mediated transport, innate immunity, redox regulation, and metabolic processes. Here, we show that algal symbionts can be transferred vertically from algal-bearing overwintering gemmules to adult sponges, and that their proliferation is enhanced by light. Sponges grown under light conditions harbored higher algal loads than those in the dark; however, algae were still able to proliferate and persist in sponges reared in the dark, occupying similar spatial locations to those grown in light. RNA-Seq analysis of algal-bearing sponges across developmental stages in light and dark conditions revealed genetic regulatory pathways involved in the transmission and establishment of the endosymbiosis. Differential expression analysis indicated that the endocytosis and SNARE pathways regulate the internalization and transport of algae at the earliest stage of hatching under light conditions and later in development under dark conditions, potentially contributing to the recruitment of endosymbiotic algae. In sponges hatched in the dark, genes involved in vesicle acidification are regulated, alongside changes in the expression of genes in the pentose phosphate pathway - a key metabolic route involved in redox homeostasis and circadian rhythm regulation via NADPH metabolism, is observed. E. muelleri serves as a versatile model system, supported by robust genomic and transcriptomic resources, for studying host-symbiont interactions. It offers a unique opportunity to investigate the molecular signaling and environmental factors that shape symbiosis in a system where the host can exist with or without algal endosymbionts, symbionts can be acquired either horizontally or vertically, and proliferation of the algae can occur with or without photosynthesis.

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Algal Holobionts

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