Microbial Environment Affects Innate Immunity in Two Closely Related Earthworm Species Eisenia andrei and Eisenia fetida

Dvořák, Jiří; Mančíková, Veronika; Pižl, Václav; Elhottová, Dana; Šilerová, Marcela; Roubalová, Radka; Škanta, František; Procházková, Petra; Bilej, Martin

doi:10.1371/journal.pone.0079257

Cited by 28 publications

(20 citation statements)

References 29 publications

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“…Earthworms, especially E . fetida have been studied extensively as a model for invertebrate innate immunity [ 87 ], but the role of SIAE has never been reported. Sialidase (SIAE) showed two paralogs with divergent expression pattern at all time points in the regenerated tissue, compared to the adjacent tissue.…”

Section: Discussionmentioning

confidence: 99%

Large scale changes in the transcriptome of Eisenia fetida during regeneration

et al. 2018

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Earthworms show a wide spectrum of regenerative potential with certain species like Eisenia fetida capable of regenerating more than two-thirds of their body while other closely related species, such as Paranais litoralis seem to have lost this ability. Earthworms belong to the phylum Annelida, in which the genomes of the marine oligochaete Capitella telata and the freshwater leech Helobdella robusta have been sequenced and studied. Herein, we report the transcriptomic changes in Eisenia fetida (Indian isolate) during regeneration. Following injury, E. fetida regenerates the posterior segments in a time spanning several weeks. We analyzed gene expression changes both in the newly regenerating cells and in the adjacent tissue, at early (15days post amputation), intermediate (20days post amputation) and late (30 days post amputation) by RNAseq based de novo assembly and comparison of transcriptomes. We also generated a draft genome sequence of this terrestrial red worm using short reads and mate-pair reads. An in-depth analysis of the miRNome of the worm showed that many miRNA gene families have undergone extensive duplications. Sox4, a master regulator of TGF-beta mediated epithelial-mesenchymal transition was induced in the newly regenerated tissue. Genes for several proteins such as sialidases and neurotrophins were identified amongst the differentially expressed transcripts. The regeneration of the ventral nerve cord was also accompanied by the induction of nerve growth factor and neurofilament genes. We identified 315 novel differentially expressed transcripts in the transcriptome, that have no homolog in any other species. Surprisingly, 82% of these novel differentially expressed transcripts showed poor potential for coding proteins, suggesting that novel ncRNAs may play a critical role in regeneration of earthworm.

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Section: Discussionmentioning

confidence: 99%

Large scale changes in the transcriptome of Eisenia fetida during regeneration

et al. 2018

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“…[ 4 – 7 ]), and are widely used as models for basic studies in vermicomposting (e.g. [ 8 , 9 ]), and biomedicine [ 10 – 12 ]. Because the molecular-genetic platforms used in these studies are both sensitive and especially specific, it is crucial that the two eco-physiologically similar commonly used species, Eisenia andrei ( Ea ; ‘red worms’) and E .…”

Section: Introductionmentioning

confidence: 99%

The existence of fertile hybrids of closely related model earthworm species, Eisenia andrei and E. fetida

et al. 2018

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Lumbricid earthworms Eisenia andrei (Ea) and E. fetida (Ef) are simultaneous hermaphrodites with reciprocal insemination capable of self-fertilization while the existence of hybridization of these two species was still debatable. During the present investigation fertile hybrids of Ea and Ef were detected. Virgin specimens of Ea and Ef were laboratory crossed (Ea+Ef) and their progeny was doubly identified. 1 –identified by species-specific maternally derived haploid mitochondrial DNA sequences of the COI gene being either ‘a’ for worms hatched from Ea ova or ‘f’ for worms hatched from Ef ova. 2 –identified by the diploid maternal/paternal nuclear DNA sequences of 28s rRNA gene being either ‘AA’ for Ea, ‘FF’ for Ef, or AF/FA for their hybrids derived either from the ‘aA’ or ‘fF’ ova, respectively. Among offspring of Ea+Ef pairs in F1 generation there were mainly aAA and fFF earthworms resulted from the facilitated self-fertilization and some aAF hybrids from aA ova but none fFA hybrids from fF ova. In F2 generation resulting from aAF hybrids mated with aAA a new generations of aAA and aAF hybrids were noticed, while aAF hybrids mated with fFF gave fFF and both aAF and fFA hybrids. Hybrids intercrossed together produced plenty of cocoons but no hatchlings independently whether aAF+aAF or aAF+fFA were mated. These results indicated that Ea and Ef species, easy to maintain in laboratory and commonly used as convenient models in biomedicine and ecotoxicology, may also serve in studies on molecular basis of interspecific barriers and mechanisms of introgression and speciation. Hypothetically, their asymmetrical hybridization can be modified by some external factors.

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“…In mammalian genomes, lysosomal and cytosolic isoforms of sialic acid 9-O-acetylesterase catalyze the removal of 9-O-acetylation and play an important role in auto-immunity and B-cell differentiation [61][62][63] . Earthworms, especially E. fetida have been studied extensively as a model for invertebrate innate immunity 64 , but the role of SIAE has never been reported. The SIAE gene had no known ortholog in the C. elegans and Drosophila melanogaster genomes, but genomic analysis revealed the presence of two closely related sialidase genes in the earthworm genome, occuring on two distinct contigs (Fig.…”

Section: Regeneration Of Blood and Immune Cellsmentioning

confidence: 99%

Insights into regeneration from the genome, transcriptome and metagenome analysis ofEisenia fetida

Bhambri

Dhaunta

Patel

et al. 2017

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Earthworms show a wide spectrum of regenerative potential with certain species like Eisenia fetida capable of regenerating more than two-thirds of their body while other closely related species, such as Paranais litoralis seem to have lost this ability. Earthworms belong to the phylum annelida, in which the genomes of the marine oligochaete Capitella telata, and the freshwater leech Helobdella robusta have been sequenced and studied. The terrestrial annelids, in spite of their ecological relevance and unique biochemical repertoire, are represented by a single rough genome draft of Eisenia fetida (North American isolate), which suggested that extensive duplications have led to a large number of HOX genes in this annelid. Herein, we report the draft genome sequence of Eisenia fetida (Indian isolate), a terrestrial redworm widely used for vermicomposting assembled using short reads and mate-pair reads. An in-depth analysis of the miRNome of the worm, showed that many miRNA gene families have also undergone extensive duplications. Genes for several important proteins such as sialidases and neurotrophins were identified by RNA sequencing of tissue samples. We also used de novo assembled RNA-Seq data to identify genes that are differentially expressed during regeneration, both in the newly regenerating cells and in the adjacent tissue. Sox4, a master regulator of TGF-beta induced epithelial-mesenchymal transition was induced in the newly regenerated tissue. The regeneration of the ventral nerve cord was also accompanied by the induction of nerve growth factor and neurofilament genes. The metagenome of the worm, characterized using 16S rRNA sequencing, revealed the identity of several bacterial species that reside in the nephridia of the worm. Comparison of the bodywall and cocoon metagenomes showed exclusion of hereditary symbionts in the regenerated tissue. In summary, we present extensive genome, transcriptome and metagenome data to establish the transcriptome and metagenome dynamics during regeneration.

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Microbial Environment Affects Innate Immunity in Two Closely Related Earthworm Species Eisenia andrei and Eisenia fetida

Cited by 28 publications

References 29 publications

Large scale changes in the transcriptome of Eisenia fetida during regeneration

Large scale changes in the transcriptome of Eisenia fetida during regeneration

The existence of fertile hybrids of closely related model earthworm species, Eisenia andrei and E. fetida

Insights into regeneration from the genome, transcriptome and metagenome analysis ofEisenia fetida

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