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Transcriptome Analysis Elucidates the Key Responses of Bryozoan Fredericella sultana during the Development of Tetracapsuloides bryosalmonae (Myxozoa).

ABSTRACT: Bryozoans are sessile, filter-feeding, and colony-building invertebrate organisms. Fredericella sultana is a well known primary host of the myxozoan parasite Tetracapsuloides bryosalmonae. There have been no attempts to identify the cellular responses induced in F. sultana during the T. bryosalmonae development. We therefore performed transcriptome analysis with the aim of identifying candidate genes and biological pathways of F. sultana involved in the response to T. bryosalmonae. A total of 1166 differentially up- and downregulated genes were identified in the infected F. sultana. Gene ontology of biological processes of upregulated genes pointed to the involvement of the innate immune response, establishment of protein localization, and ribosome biogenesis, while the downregulated genes were involved in mitotic spindle assembly, viral entry into the host cell, and response to nitric oxide. Eukaryotic Initiation Factor 2 signaling was identified as a top canonical pathway and MYCN as a top upstream regulator in the differentially expressed genes. Our study provides the first transcriptional profiling data on the F. sultana zooid's response to T. bryosalmonae. Pathways and upstream regulators help us to understand the complex interplay in the infected F. sultana. The results will facilitate the elucidation of innate immune mechanisms of bryozoan and will lay a foundation for further analyses on bryozoan-responsive candidate genes, which will be an important resource for the comparative analysis of gene expression in bryozoans.

SUBMITTER: Kumar G

PROVIDER: S-EPMC7460649 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Transcriptome Analysis Elucidates the Key Responses of Bryozoan Fredericella sultana during the Development of Tetracapsuloides bryosalmonae (Myxozoa).

Kumar Gokhlesh G Ertl Reinhard R Bartholomew Jerri L JL El-Matbouli Mansour M

International journal of molecular sciences 20200817 16

Bryozoans are sessile, filter-feeding, and colony-building invertebrate organisms. Fredericella sultana is a well known primary host of the myxozoan parasite Tetracapsuloides bryosalmonae. There have been no attempts to identify the cellular responses induced in F. sultana during the T. bryosalmonae development. We therefore performed transcriptome analysis with the aim of identifying candidate genes and biological pathways of F. sultana involved in the respons ...[more]

PMID: 32824626

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Project description:Proliferative kidney disease (PKD) caused by the myxozoan parasite Tetracapsuloides bryosalmonae is one of the most serious infectious diseases negatively impacting farmed and wild salmonids throughout Europe and North America. PKD pathogenesis results in a massive B cell proliferation and dysregulation with aberrant immunoglobulin production and plasma cell differentiation along with a decrease in myeloid cells and inhibition of innate pathways. Despite the huge immunopathological reaction in the kidney during infection, under specific conditions, fish can survive and return to full fitness. Fish are unique in this ability to recover renal structure and functionality from extensive tissue damage in contrast to mammals. However, only limited knowledge exists regarding the host immune response coinciding with PKD recovery. Moreover, almost no studies of the immune response during disease recovery exist in fish. We utilized the rainbow trout-T. bryosalmonae system as an immunological model of disease recovery. Our results demonstrated that recovery is preceded by an intense immune response at the transcript level, decreasing parasite burden, and an increased degree of kidney inflammation. Later in the recovery phase, the immune response transpired with a significant decrease in lymphocytes and an increase in myeloid cells. These lymphocytes populations contained lower levels of B cells comparative to the control in the anterior and posterior kidney. Additionally, there was downregulation of several transcripts used as markers for plasma cells (blimp1, igt sec, igm sec, igd sec, and cd38) and T cell subsets (cd4, cd8α, cd8β, and tcrβ). The decrease in these T cell transcripts significantly correlated with decreasing parasite intensity. Alternatively, there was strong upregulation of pax-5 and igt mem. This suggests a change in B cell processes during the recovery phase relative to clinical PKD may be necessary for the host to re-establish homeostasis in terms of an arrest in the dominant antibody like response transitioning to a transcriptional profile associated with resting B cells. The knowledge generated here in combination with earlier studies illuminates the full power of analyzing the entire trajectory of disease from the normal healthy state to recovery enabling the measurement of an immune response to pinpoint a specific disease stage.

Dataset Information

Transcriptome Analysis Elucidates the Key Responses of Bryozoan Fredericella sultana during the Development of Tetracapsuloides bryosalmonae (Myxozoa).

Publications

Transcriptome Analysis Elucidates the Key Responses of Bryozoan <i>Fredericella sultana</i> during the Development of <i>Tetracapsuloides bryosalmonae</i> (Myxozoa).

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