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Transcriptomes reveal expression of hemoglobins throughout insects and other Hexapoda.

ABSTRACT: Insects have long been thought to largely not require hemoglobins, with some notable exceptions like the red hemolymph of chironomid larvae. The tubular, branching network of tracheae in hexapods is traditionally considered sufficient for their respiration. Where hemoglobins do occur sporadically in plants and animals, they are believed to be either convergent, or because they are ancient in origin and their expression is lost in many clades. Our comprehensive analysis of 845 Hexapod transcriptomes, totaling over 38 Gbases, revealed the expression of hemoglobins in all 32 orders of hexapods, including the 29 recognized orders of insects. Discovery and identification of 1333 putative hemoglobins were achieved with target-gene BLAST searches of the NCBI TSA database, verifying functional residues, secondary- and tertiary-structure predictions, and localization predictions based on machine learning. While the majority of these hemoglobins are intracellular, extracellular ones were recovered in 38 species. Gene trees were constructed via multiple-sequence alignments and phylogenetic analyses. These indicate duplication events within insects and a monophyletic grouping of hemoglobins outside other globin clades, for which we propose the term insectahemoglobins. These hemoglobins are phylogenetically adjacent and appear structurally convergent with the clade of chordate myoglobins, cytoglobins, and hemoglobins. Their derivation and co-option from early neuroglobins may explain the widespread nature of hemoglobins in various kingdoms and phyla. These results will guide future work involving genome comparisons to transcriptome results, experimental investigations of gene expression, cell and tissue localization, and gas binding properties, all of which are needed to further illuminate the complex respiratory adaptations in insects.

SUBMITTER: Herhold HW

PROVIDER: S-EPMC7274415 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The dimorphic fungus Histoplasma capsulatum causes respiratory and systemic disease in mammalian hosts by expression of factors that enable survival within phagocytic cells of the immune system. Histoplasma's dimorphism is distinguished by growth either as avirulent mycelia or as pathogenic yeast. Geographically distinct strains of Histoplasma differ in their relative virulence in mammalian hosts and in production of and requirement for specific virulence factors. The close similarity in the genome sequences of these diverse strains suggests that phenotypic variations result from differences in gene expression rather than gene content. To provide insight into how the transcriptional program translates into morphological variation and the pathogenic lifestyle, we compared the transcriptional profile of the pathogenic yeast phase and the non-pathogenic mycelial phase of two clinical isolates of Histoplasma.To overcome inaccuracies in ab initio genome annotation of the Histoplasma genome, we used RNA-seq methodology to generate gene structure models based on experimental evidence. Quantitative analyses of the sequencing reads revealed 6% to 9% of genes are differentially regulated between the two phases. RNA-seq-based mRNA quantitation was strongly correlated with gene expression levels determined by quantitative RT-PCR. Comparison of the yeast-phase transcriptomes between strains showed 7.6% of all genes have lineage-specific expression differences including genes contributing, or potentially related, to pathogenesis. GFP-transcriptional fusions and their introduction into both strain backgrounds revealed that the difference in transcriptional activity of individual genes reflects both variations in the cis- and trans-acting factors between Histoplasma strains.Comparison of the yeast and mycelial transcriptomes highlights genes encoding virulence factors as well as those involved in protein glycosylation, alternative metabolism, lipid remodeling, and cell wall glycanases that may contribute to Histoplasma pathogenesis. These studies lay an essential foundation for understanding how gene expression variations contribute to the strain- and phase-specific virulence differences of Histoplasma.

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Transcriptomes reveal expression of hemoglobins throughout insects and other Hexapoda.

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