scholarly journals Immune gene regulation in the gut during metamorphosis in a holo- versus a hemimetabolous insect

2019 ◽  
Vol 374 (1783) ◽  
pp. 20190073 ◽  
Author(s):  
Paul R. Johnston ◽  
Véronique Paris ◽  
Jens Rolff

During metamorphosis, holometabolous insects completely replace the larval gut and must control the microbiota to avoid septicaemia. Rapid induction of bactericidal activity in the insect gut at the onset of pupation has been described in numerous orders of the Holometabola and is best-studied in the Lepidoptera where it is under control of the 20-hydroxyecdysone (20E) moulting pathway. Here, using RNAseq, we compare the expression of immune effector genes in the gut during metamorphosis in a holometabolous ( Galleria mellonella ) and a hemimetabolous insect ( Gryllus bimaculatus ). We find that in G. mellonella , the expression of numerous immune effectors and the transcription factor GmEts are upregulated, with peak expression of three antimicrobial peptides (AMPs) and a lysozyme coinciding with delamination of the larval gut. By contrast, no such upregulation was detectable in the hemimetabolous Gr. bimaculatus . These findings support the idea that the upregulation of immune effectors at the onset of complete metamorphosis is an adaptive response, which controls the microbiota during gut replacement. This article is part of the theme issue ‘The evolution of complete metamorphosis’.

2019 ◽  
Vol 374 (1783) ◽  
pp. 20190225 ◽  
Author(s):  
Yoshiyasu Ishimaru ◽  
Sayuri Tomonari ◽  
Takahito Watanabe ◽  
Sumihare Noji ◽  
Taro Mito

Juvenile hormones and the genetic interaction between the transcription factors Krüppel homologue 1 ( Kr-h1 ) and Broad ( Br ) regulate the transformation of insects from immature to adult forms in both types of metamorphosis (holometaboly with a pupal stage versus hemimetaboly with no pupal stage); however, knowledge about the exact instar in which this occurs is limited. Using the hemimetabolous cricket Gryllus bimaculatus ( Gb ), we demonstrate that a genetic interaction occurs among Gb ′ Kr-h1 , Gb ′ Br and the adult-specifier transcription factor Gb ′ E93 from the sixth to final (eighth) nymphal instar. Gb ′ Kr-h1 and Gb ′ Br mRNAs were strongly expressed in the abdominal tissues of sixth instar nymphs, with precocious adult moults being induced by Gb ′ Kr-h1 or Gb ′ Br knockdown in the sixth instar. The depletion of Gb ′ Kr-h1 or Gb ′ Br upregulates Gb ′ E93 in the sixth instar. By contrast, Gb ′ E93 knockdown at the sixth instar prevents nymphs transitioning to adults, instead producing supernumerary nymphs. Gb ′ E93 also represses Gb ′ Kr-h1 and Gb ′ Br expression in the penultimate nymphal instar, demonstrating its important role in adult differentiation. Our results suggest that the regulatory mechanisms underlying the pupal transition in holometabolous insects are evolutionarily conserved in hemimetabolous G . bimaculatus , with the penultimate and final nymphal periods being equivalent to the pupal stage. This article is part of the theme issue ‘The evolution of complete metamorphosis’.


2021 ◽  
Vol 17 (1) ◽  
Author(s):  
Rodrigo Díaz ◽  
José Troncoso ◽  
Eva Jakob ◽  
Stanko Skugor

Abstract Background Vertebrate hosts limit the availability of iron to microbial pathogens in order to nutritionally starve the invaders. The impact of iron deficiency induced by the iron chelator deferoxamine mesylate (DFO) was investigated in Atlantic salmon SHK-1 cells infected with the facultative intracellular bacterium Piscirickettsia salmonis. Results Effects of the DFO treatment and P. salmonis on SHK-1 cells were gaged by assessing cytopathic effects, bacterial load and activity, and gene expression profiles of eight immune biomarkers at 4- and 7-days post infection (dpi) in the control group, groups receiving single treatments (DFO or P. salmonis) and their combination. The chelator appears to be well-tolerated by host cells, while it had a negative impact on the number of bacterial cells and associated cytotoxicity. DFO alone had minor effects on gene expression of SHK-1 cells, including an early activation of IL-1β at 4 dpi. In contrast to few moderate changes induced by single treatments (either infection or chelator), most genes had highest upregulation in the infected groups receiving DFO. The mildest induction of hepcidin-1 (antimicrobial peptide precursor and regulator of iron homeostasis) was observed in cells exposed to DFO alone, followed by P. salmonis infected cells while the addition of DFO to infected cells further increased the mRNA abundance of this gene. Transcripts encoding TNF-α (immune signaling) and iNOS (immune effector) showed sustained increase at both time points in this group while cathelicidin-1 (immune effector) and IL-8 (immune signaling) were upregulated at 7 dpi. The stimulation of protective gene responses seen in infected cultures supplemented with DFO coincided with the reduction of bacterial load and activity (judged by the expression of P. salmonis 16S rRNA), and damage to cultured host cells. Conclusion The absence of immune gene activation under normal iron conditions suggests modulation of host responses by P. salmonis. The negative effect of iron deficiency on bacteria likely allowed host cells to respond in a more protective manner to the infection, further decreasing its progression. Presented findings encourage in vivo exploration of iron chelators as a promising strategy against piscirickettsiosis.


Author(s):  
Iryna Yakovenko ◽  
Asaf Donnyo ◽  
Or Ioscovich ◽  
Benyamin Rosental ◽  
Matan Oren

Sea urchins are long-living invertebrates with a complex immune system which includes extended families of immune receptors. A central immune gene family in the sea urchins encodes for the Transformer (Trf) proteins. The Trf family was so far studied mainly in the purple sea urchin Strongylocentrotus purpuratus. In this study, we explored this protein family in the Mediterranean Sea urchin Paracentrotus lividus. The PlTrf genes and predicted proteins were found to be highly diverse and showed a typical Trf size range and structure. We found that P. lividus coelomocytes and hemolymph contain different PlTrf protein repertoires with a shared subset which specifically bind E. coli bacteria. Using FACS, we identified five different P. lividus coelomocyte sub-populations with cell surface Trf protein expression. The relative abundance of the Trf-positive cells sharply increased following immune challenge with E. coli bacteria, but not following challenge with LPS or sea urchin pathogen V. penaeicida. Finally, we demonstrated that the phagocytosis of E. coli bacteria by P. lividus phagocytes is mediated through the hemolymph and is inhibited by blocking Trf activity with anti-Trf antibodies. Together, our results suggest collaboration between cellular and humoral Trf-mediated effector arms in the P. lividus specific immune response to pathogens.


2018 ◽  
Vol 6 (7) ◽  
Author(s):  
Joon-hui Chung ◽  
Haeyoung Jeong ◽  
Choong-Min Ryu

ABSTRACT Enterobacter cancerogenus CR-Eb1 and Enterococcus sp. CR-Ec1 were isolated from the larval gut of Galleria mellonella , the greater wax moth. Here, we report the completed and annotated genome sequences of insect gut-dwelling bacteria.


2019 ◽  
Vol 374 (1783) ◽  
pp. 20190069 ◽  
Author(s):  
Carita Lindstedt ◽  
Liam Murphy ◽  
Johanna Mappes

Antipredator strategies of the pupal stage in insects have received little attention in comparison to larval or adult stages. This is despite the fact that predation risk can be high during the pupal stage, making it a critical stage for subsequent fitness. The immobile pupae are not, however, defenceless; a wide range of antipredator strategies have evolved against invertebrate and vertebrate predators. The most common strategy seems to be ‘avoiding encounters with predators' by actively hiding in vegetation and soil or via cryptic coloration and masquerade. Pupae have also evolved behavioural and secondary defences such as defensive toxins, physical defences or deimatic movements and sounds. Interestingly, warning coloration used to advertise unprofitability has evolved very rarely, even though the pupal stage often contains defensive toxins in chemically defended species. In some species, pupae gain protection from conspecifics or mimic chemical and auditory signals and thereby manipulate other species to protect them. Our literature survey highlights the importance of studying selection pressures across an individual's life stages to predict how ontogenetic variation in selective environments shapes individual fitness and population dynamics in insects. Finally, we also suggest interesting avenues for future research to pursue. This article is part of the theme issue ‘The evolution of complete metamorphosis’.


2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Guillem Ylla ◽  
Taro Nakamura ◽  
Takehiko Itoh ◽  
Rei Kajitani ◽  
Atsushi Toyoda ◽  
...  

AbstractMost of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation. In contrast, Hemimetabolous insects undergo the presumed ancestral process of incomplete metamorphosis, and have larger genomes with high levels of DNA methylation. Hemimetabolous species from the Orthopteran order (grasshoppers and crickets) have some of the largest known insect genomes. What drives the evolution of these unusual insect genome sizes, remains unknown. Here we report the sequencing, assembly and annotation of the 1.66-Gb genome of the Mediterranean field cricket Gryllus bimaculatus, and the annotation of the 1.60-Gb genome of the Hawaiian cricket Laupala kohalensis. We compare these two cricket genomes with those of 14 additional insects and find evidence that hemimetabolous genomes expanded due to transposable element activity. Based on the ratio of observed to expected CpG sites, we find higher conservation and stronger purifying selection of methylated genes than non-methylated genes. Finally, our analysis suggests an expansion of the pickpocket class V gene family in crickets, which we speculate might play a role in the evolution of cricket courtship, including their characteristic chirping.


2019 ◽  
Vol 374 (1783) ◽  
pp. 20190070 ◽  
Author(s):  
James W. Truman ◽  
Lynn M. Riddiford

Developmental, genetic and endocrine data from diverse taxa provide insight into the evolution of insect metamorphosis. We equate the larva–pupa–adult of the Holometabola to the pronymph–nymph–adult of hemimetabolous insects. The hemimetabolous pronymph is a cryptic embryonic stage with unique endocrinology and behavioural modifications that probably served as preadaptations for the larva. It develops in the absence of juvenile hormone (JH) as embryonic primordia undergo patterning and morphogenesis, the processes that were arrested for the evolution of the larva. Embryonic JH then drives tissue differentiation and nymph formation. Experimental treatment of pronymphs with JH terminates patterning and induces differentiation, mimicking the processes that occurred during the evolution of the larva. Unpatterned portions of primordia persist in the larva, becoming imaginal discs that form pupal and adult structures. Key transcription factors are associated with the holometabolous life stages: Krüppel-homolog 1 ( Kr-h1 ) in the larva, broad in the pupa and E93 in the adult. Kr-h1 mediates JH action and is found whenever JH acts, while the other two genes direct the formation of their corresponding stages. In hemimetabolous forms, the pronymph has low Broad expression, followed by Broad expression through the nymphal moults, then a switch to E93 to form the adult. This article is part of the theme issue ‘The evolution of complete metamorphosis’.


2019 ◽  
Vol 374 (1783) ◽  
pp. 20190065 ◽  
Author(s):  
Gianluca Tettamanti ◽  
Morena Casartelli

In insects that undergo complete metamorphosis, cell death is essential for reshaping or removing larval tissues and organs, thus contributing to formation of the adult's body structure. In the last few decades, the study of metamorphosis in Lepidoptera and Diptera has provided broad information on the tissue remodelling processes that occur during larva–pupa–adult transition and made it possible to unravel the underlying regulatory pathways. This review summarizes recent knowledge on cell death mechanisms in Lepidoptera and other holometabolous insects, highlighting similarities and differences with Drosophila melanogaster , and discusses the role of apoptosis and autophagy in this developmental setting. This article is part of the theme issue ‘The evolution of complete metamorphosis'.


BMC Genomics ◽  
2011 ◽  
Vol 12 (1) ◽  
Author(s):  
Heiko Vogel ◽  
Boran Altincicek ◽  
Gernot Glöckner ◽  
Andreas Vilcinskas

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