Physiological and Dual Transcriptional Analysis of Microalga Graesiella emersonii–Amoeboaphelidium protococcarum Pathosystem Uncovers Conserved Defense Response and Robust Pathogenicity

Abstract

The underlying mechanisms of microalgal host–pathogen interactions remain largely unknown. In this study, we applied physiological and simultaneous dual transcriptomic analysis to characterize the microalga Graesiella emersonii–Amoeboaphelidium protococcarum interaction. Three infection stages were determined according to infection rate and physiological features. Dual RNA-seq results showed that the genes expression of G. emersonii and A. protococcarum were strongly dynamically regulated during the infection. For microalgal hosts, similar to plant defense response, the expression of defense genes involved in the pattern recognition receptors, large heat shock proteins, and reactive oxygen scavenging enzymes (glutathione, ferritin, and catalase) were significantly upregulated during infection. However, some genes encoding resistance proteins (R proteins) with a leucine-rich repeat domain exhibited no significant changes during infection. For endoparasite A. protococcarum, genes for carbohydrate-active enzymes, pathogen–host interactions, and putative effectors were significantly upregulated during infection. Furthermore, the genes in cluster II were significantly enriched in pathways associated with the modulation of vacuole transport, including endocytosis, phagosome, ubiquitin-mediated proteolysis, and SNARE interactions in vesicular transport pathways. These results suggest that G. emersonii has a conserved defense system against pathogen and that endoparasite A. protococcarum possesses a robust pathogenicity to infect the host. Our study characterizes the first transcriptomic profile of microalgae–endoparasite interaction, providing a new promising basis for complete understanding of the algal host defense strategies and parasite pathogenicity.

Associated bacterial microbiome responds opportunistic once algal host Scenedesmus vacuolatus is attacked by endoparasite Amoeboaphelidium protococcarum

“…1 ), while fungal PGs peaked with 4 DPI and flatten until 7 DPI. The abundance of fungal PGs matches the reported reproduction cycle of A. protococcarum , which includes intrusion of host cells, phagocytosis of the host cytoplasm and maturation of spores within 3–5 DPI 32 , 34 .…”

“…The results included a predicted proteome, covering full life-cycle data including cellulases, which were likely involved in algal cell-wall penetration, and enzymes involved in chitin biosynthesis, indicating typical fungal metabolism. The responses and defense reactions to pathogen infection of A. protococcarum on the green microalga Graesiella emersonii have just recently been investigated 34 . The defense of G. emersonii included pattern recognition receptors, large heat shock proteins, and reactive oxygen scavenging enzymes.…”

Folate-mediated one-carbon metabolism as a potential antifungal target for the sustainable cultivation of microalga Haematococcus pluvialis

“…Examples of using such approaches to facilitate understanding the metabolic pathways required for fungal pathogenicity show that by comparative analysis of the genomes of the fungal pathogens and the oleaginous algal host Nannochloropsis oceanica , the differences in the key enzymes and genetic structure of the sterol biosynthetic pathway can be identified as targets for commercial fungicides [ 22 ]. And by transcriptomic analysis of the interaction processes between the microalga Graesiella emersonii and its endoparasite Amoeboaphelidium protococcarum, novel insights into robust pathogenicity of the parasite can be gained [ 14 ]. Recently, metabolomic analysis has demonstrated that the secondary metabolites, such as 3-hydroxyanthranilic acid and hordenine, can trigger the oxidative burst in H. pluvialis cells and can be used by P. sedebokerense to facilitate infection [ 69 ].…”