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Aguirre Carrion, P. J.

Publications and source records attributed to Aguirre Carrion, P. J..

3 recordsLinked to original sources

Nutrient deprivation differentially affects gene expression, immunity, and pathogen susceptibility across symbiotic states in a model cnidarian

Mutualistic symbioses between cnidarians and photosynthetic algae are modulated by complex interactions between host immunity and environmental conditions. Here, we investigate how symbiosis interacts with nutrient limitation to influence gene expression and stress response programming in the sea anemone Exaiptasia pallida (Aiptasia). Transcriptomic responses to starvation were similar between symbiotic and aposymbiotic Aiptasia; however, aposymbiotic anemone responses were stronger. Starved Aiptasia of both symbiotic states exhibited increased protein levels of immune-related transcription factor NF-{kappa}B, its associated gene pathways, and putative target genes. However, this starvation-induced increase in NF-{kappa}B only correlated with increased immunity in symbiotic anemones. Furthermore, starvation had opposite effects on Aiptasia susceptibility to pathogen and oxidative stress challenges, suggesting distinct energetic priorities under nutrient scarce conditions. Finally, when we compared starvation responses in Aiptasia to those of a facultative coral and nonsymbiotic anemone, "defense" responses were similarly regulated in Aiptasia and the facultative coral, but not in the nonsymbiotic anemone. This pattern suggests that capacity for symbiosis influences immune responses in cnidarians. In summary, expression of certain immune pathways - including NF-{kappa}B - does not necessarily predict susceptibility to pathogens, highlighting the complexities of cnidarian immunity and the influence of symbiosis under varying energetic demands.

genomics↗

Starvation Decreases Immunity and Immune Regulatory Factor NF-κB in the Starlet Sea Anemone Nematostella vectensis

Lack of proper nutrition (malnutrition) or the complete absence of all food (starvation) have important consequences on the physiology of all organisms. In many cases, nutritional status affects immunity, but, for the most part, the relationship between nutrition and immunity has been limited to studies in vertebrates and terrestrial invertebrates. Herein, we describe a positive correlation between nutrition and immunity in the sea anemone Nematostella vectensis. Gene expression profiling of adult fed and starved anemones showed downregulation of many genes involved in nutrient metabolism and cellular respiration, as well as immune-related genes, in starved animals. Starved adult anemones also had reduced protein levels and DNA-binding activity of immunity-related transcription factor NF-{kappa}B. Starved juvenile anemones had increased sensitivity to bacterial infection and also had lower NF-{kappa}B protein levels, as compared to fed controls. Weighted Gene Correlation Network Analysis (WGCNA) revealed significantly correlated gene networks that were inversely associated with starvation. Based on the WGCNA and a reporter gene assay, we identified TRAF3 as a likely NF-{kappa}B target gene in N. vectensis. Overall, these experiments demonstrate a correlation between nutrition and immunity in a basal marine metazoan, and the results have implications for the survival of marine organisms as they encounter changing environments. Significance StatementAdequate nutrition is required to sustain proper biological function. One factor threatening many marine organisms, as a result of modern day anthropogenic environmental changes, is nutrient availability. Here, we characterize transcriptional changes following food deprivation in the cnidarian model sea anemone Nematostella vectensis. We show that starvation is correlated with decreased expression of genes associated with nutrient metabolism and immunity, among others. Moreover, starvation reduces the level of expression and activity of immune regulatory transcription factor NF-{kappa}B and causes anemones to have increased susceptibility to bacterial infection. These results demonstrate that this basal organism responds at the transcriptional level to the absence of food, and that, in addition to changes in metabolic factors, starvation leads to a reduction in immunity.

immunology↗

Diversification of Transcription Factor NF-κB in Protists

In this report, we investigate the evolution of transcription factor NF-{kappa}B by examining its structure, activity, and regulation in two protists using phylogenetic, cellular, and biochemical techniques. In Capsaspora owczarzaki (Co), we find that full-length NF-{kappa}B has an N-terminal DNA-binding domain and a C-terminal Ankyrin (ANK) repeat inhibitory domain, and its DNA-binding activity is more similar to metazoan NF-{kappa}B rather than Rel proteins. As with mammalian NF-{kappa}B proteins, removal of the ANK repeats is required for Co-NF-{kappa}B to enter the nucleus, bind DNA, and activate transcription. However, C-terminal processing of Co-NF-{kappa}B is not induced by co-expression of IKK in human cells. Exogenously expressed Co-NF-{kappa}B localizes to the nucleus in Co cells. NF-{kappa}B mRNA and DNA-binding levels differ across three life stages of Capsaspora, suggesting distinct roles for NF-{kappa}B in these life stages. RNA-seq and GO analyses identify possible gene targets and biological functions of Co-NF-{kappa}B. We also show that three NF-{kappa}B-like proteins from the choanoflagellate Acanthoeca spectabilis (As) all consist of primarily the N-terminal conserved Rel Homology domain sequences of NF-{kappa}B, and lack C-terminal ANK repeats. All three As-NF-{kappa}B proteins constitutively enter the nucleus of human and Co cells, but differ in their DNA-binding and transcriptional activation activities. Furthermore, all three As-NF-{kappa}B proteins can form heterodimers, indicating that NF-{kappa}B diversified into multi-subunit families at least two times during evolution. Overall, these results present the first functional characterization of NF-{kappa}B in a taxonomic kingdom other than Animalia and provide information about the evolution and diversification of this biologically important transcription factor. SignificanceThese results represent the first functional characterization of the biologically important transcription factor NF-{kappa}B in a taxonomic kingdom other than Animalia. As such, they provide information on the evolutionary origins and basal diversification of NF-{kappa}B outside of metazoans. These results suggest that NF-{kappa}B plays life stage-specific roles in Capsaspora, the closest unicellular ancestor to all metazoans. Finally, the analysis of three NF-{kappa}B proteins in a single choanoflagellate indicates that choanoflagellates have subclasses of NF-{kappa}Bs, which can form heterodimers, suggesting that NF-{kappa}B subunit expansion and diversification has occurred at least twice in evolution.

cell biology↗