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Front Genet
2021 Jan 01;12:795706. doi: 10.3389/fgene.2021.795706.
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Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions.
Chan J
,
Wang L
,
Li L
,
Mu K
,
Bushek D
,
Xu Y
,
Guo X
,
Zhang G
,
Zhang L
.
Abstract
Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.
FIGURE 1. Schematic diagram of experimental design. FSW, filtered seawater.
FIGURE 2. Transcriptional changes induced by P. marinus in C. virginica.
(A), Volcano plots of transcriptional change under short-term and long-term P. marinus challenge. Blue points represent downregulated genes, red points represent upregulated genes, and black points represent non-differentially expressed genes. (B), Functional annotation of differentially expressed genes under P. marinus challenge. (C), Immune-related genes significantly up-regulated after dermo challenge.
FIGURE 3. Comparative transcriptome analysis between C. gigas and C. virginica under P. marinus challenge. (A), Number of immune-related genes identified (Left) and number of immune-related genes differentially expressed (Right) in C. gigas (Cg) and C. virginica (Cv). (B), Venn diagrams of differentially expressed immune genes under P. marinus challenge between the two oyster species. (C), Unique and differentially expressed immune genes induced by P. marinus in two oyster species. (D), Transcriptional change of differentially expressed immune genes shared by two oyster species, including pattern recognition receptors (e.g., TLRs) and immune effectors (e.g., TRAFs).
FIGURE 4. GO enrichment analysis of the differentially expressed genes after Dermo challenge between C. virginica
(A) and C. gigas
(B). Red and blue columns represent functional enrichments of up-regulated and down-regulated genes, respectively.
FIGURE 5. Expansion of TLRs and divergent expression patterns under P. marinus challenge between C. gigas and C. virginica.
(A), Phylogenetic tree constructed with the maximum likelihood method showing lineage-specific expansion of TLRs in C. gigas (red font) and C. virginica (blue font). Red and blue asterisks represent the differentially expressed TLRs in C. gigas and C. virginica, respectively. (B), Comparison of TLRs with different domain architectures in: human (Homo sapiens-Hs), sea urchin (Strongylocentrotus purpuratus-SP), fruit fly (Drosophila melanogaster-Dm), Pacific oyster (Crassostrea gigas-Cg), Eastern oyster (Crassostrea virginica-Cv), and staghorn coral (Acropora digitifera-Ad). LRRCT in red, LRRNT in blue and LRR in yellow. Toll/interleukin-1 receptor (TIR) domains are shown as gold triangles. (C), Diverse expression pattern of the differentially expressed TLRs, marked with asterisks in (A), during P. marinus challenge in C. gigas
(Top) and C. virginica
(Bottom).
FIGURE 6. Tandem duplication and positive selection of TLRs in C. virginica. (A), Tandem repeats as the major source of TLRs duplication in C. virginica.
(B), The largest tandem repeat cluster (Top) and divergent expression patterns (Bottom) of tandemly linked TLRs in NC_035786.1 under P. marinus challenge. The wide arrows represent TLR genes, and genes with red background are differentially expressed under P. marinus challenge. A pseudogene LOC111105057 was detected in this repeat cluster. (C), Evolutionary relationships of duplicated TLRs. The calculated dN/dS (ω) values (gold) and bootstrap values are shown for each branch. The branches with ω values >1.0 are marked with red rectangle. The differential genes under P. marinus challenge that are positively selected are boxed with red dash lines. (D), Structural modeling of TLR depicting sites (blue) under positive selection. Positive selection sites (Asp27, Glu62, Asn199) are represented by black arrows.
FIGURE 7. Expansion of C1qDCs and divergent expression patterns under P. marinus challenge between C. virginica and C. gigas. (A), Phylogenetic tree constructed with the maximum likelihood method showing lineage-specific expansion of C1qDCs in C. virginica (red font) and C. gigas (gray font). Different color backgrounds represent different types of C1qDC domain composition, and the red and gray asterisks represent differentially expressed C1qDCs under P. marinus challenge in C. virginica and C. gigas, respectively. (B), Domain composition of the “galactose-binding lectin” containing C1qDC gene. (C), A C1qDC gene (LOC111120224) with “galactose-binding lectin” domain was significantly upregulated in C. virginica after P. marinus challenge.
FIGURE 8. Expansion and phylogeny of FBGDC gene family in C. virginica (red font) and C. gigas (gray font). The phylogenetic tree is constructed with the maximum likelihood method showing lineage-specific expansion of FBGDC in C. virginica (red font) and C. gigas (gray font). Different color backgrounds represent different domain composition types, and the red and gray asterisks represent differentially expressed FBGDCs under P. marinus challenge in C. virginica and C. gigas, respectively.
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