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Altered Expression of Chemosensory and Odorant Binding Proteins in Response to Fungal Infection in the Red Imported Fire Ant, Solenopsis invicta.

ABSTRACT: Social insects have evolved acute mechanisms for sensing and mitigating the spread of microbial pathogens within their communities that include complex behaviors such as grooming and sanitation. Chemical sensing involves detection and transport of olfactory and other chemicals that are mediated by at least two distinct classes of small molecular weight soluble proteins known as chemosensory- and odorant binding proteins (CSPs and OBPs, respectively) that exist as protein families in all insects. However, to date, a systematic examination of the expression of these genes involved in olfactory and other pathways to microbial infection has yet to be reported. The red imported fire ant, Solenopsis invicta, is one of the most successful invasive organisms on our planet. Here, we examined the temporal gene expression profiles of a suite of S. invicta CSPs (SiCSPs1-22) and OBPs (SiOBPs1-16) in response to infection by the broad host range fungal insect pathogen, Beauveria bassiana. Our data show that within 24 h post-infection, i.e., before the fungus has penetrated the host cuticle, the expression of SiCSPs and SiOBPs is altered (mainly increased compared to uninfected controls), followed by suppression of SiCSP and select SiOBP expression 48 h post-infection and mixed responses at 72 h post-infection. A smaller group of SiBOPs, however, appeared to respond to fungal infection, with expression of SiOBP15 consistently higher during fungal infection over the time course examined. These data indicate dynamic gene expression responses of CSPs and OBPs to fungal infection that provide clues to mechanisms that might mediate detection of microbial pathogens, triggering grooming, and nest sanitation.

SUBMITTER: Wei Z

PROVIDER: S-EPMC7970113 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAdvances in sequencing and analysis tools have facilitated discovery of many new viruses from invertebrates, including ants. Solenopsis invicta is an invasive ant that has quickly spread worldwide causing significant ecological and economic impacts. Its virome has begun to be characterized pertaining to potential use of viruses as natural enemies. Although the S. invicta virome is the best characterized among ants, most studies have been performed in its native range, with less information from invaded areas.MethodsUsing a metatranscriptome approach, we further identified and molecularly characterized virus sequences associated with S. invicta, in two introduced areas, U.S and Taiwan. The data set used here was obtained from different stages (larvae, pupa, and adults) of S. invicta life cycle. Publicly available RNA sequences from GenBank's Sequence Read Archive were downloaded and de novo assembled using CLC Genomics Workbench 20.0.1. Contigs were compared against the non-redundant protein sequences and those showing similarity to viral sequences were further analyzed.ResultsWe characterized five putative new viruses associated with S. invicta transcriptomes. Sequence comparisons revealed extensive divergence across ORFs and genomic regions with most of them sharing less than 40% amino acid identity with those closest homologous sequences previously characterized. The first negative-sense single-stranded RNA virus genomic sequences included in the orders Bunyavirales and Mononegavirales are reported. In addition, two positive single-strand virus genome sequences and one single strand DNA virus genome sequence were also identified. While the presence of a putative tenuivirus associated with S. invicta was previously suggested to be a contamination, here we characterized and present strong evidence that Solenopsis invicta virus 14 (SINV-14) is a tenui-like virus that has a long-term association with the ant. Furthermore, based on virus sequence abundance compared to housekeeping genes, phylogenetic relationships, and completeness of viral coding sequences, our results suggest that four of five virus sequences reported, those being SINV-14, SINV-15, SINV-16 and SINV-17, may be associated to viruses actively replicating in the ant S. invicta.ConclusionsThe present study expands our knowledge about viral diversity associated with S. invicta in introduced areas with potential to be used as biological control agents, which will require further biological characterization.

Project description:Purpose: We aimed to provide a basis for the adaptive mechanism and a rich resource for the discovery and identification of novel genes involved in the cold and heat stress response in Solenopsis invicta. retinal transcriptome profiling (RNA-seq) to microarray and quantitative reverse transcription polymerase chain reaction (qRT–PCR) methods and to evaluate protocols for optimal high-throughput data analysis Methods: Solenopsis invicta was reared at lab condition, and incubated at 4 different temperature for 24h (10, 20, 30 and 40℃). RNA was extracted using Trizol reagent and Illumina sequencing was performed at Macrogen. Illumina short reads were quality-filtered and Illumina-based de novo transcriptome assembly was performed. Differential Gene Expression Analysis was studied for different tempearture conditions. Results: Totally 99,085 unigenes was obtained which at least 19,154 were annotated with gene descriptions, gene ontology terms, and metabolic pathways. 86 GO functional sub-groups and 23 EggNOG terms resulted. DEGs with log2FC≥10 were screened and were compared at different temperatures. We found 203, 48 and 66 specific DEGs co-regulated at 10, 20 and 40℃, respectively compare with 30℃. Comparing transcriptome profiles for differential gene expression resulted various DE proteins and genes, including cytochrome P450, NADH dehydrogenase subunit 1, cuticle protein and HSP which have previously been reported to be involved in cold and high temperature resistance. GO analysis revealed that antioxidant activity up-regulated under high temperature stress. Conclusions: we compared the transcriptomes of S. invicta under high- and low-temperature stresses using RNA-Seq technology based on the high-throughput sequencing. Comparative transcriptome analysis identified many genes and a large number of changes were discovered in metabolic pathway through the GO and KEGG enrichment analysis. Our data will facilitate further molecular investigations and genomic research. Many high- and low-temperature significantly up-regulated genes were first identified in this study. These newly found genes may be important and necessary to RIFA overwintering and its behavior for adaptation in new environment as well as quarantine area.

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Altered Expression of Chemosensory and Odorant Binding Proteins in Response to Fungal Infection in the Red Imported Fire Ant, Solenopsis invicta.

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