Gigantic Genomes Can Provide Empirical Tests of TE Dynamics Models — An Example from Amphibians

Abstract

Transposable elements (TEs) are a major determinant of eukaryotic genome size. The collective properties of a genomic TE community reveal the history of TE/host evolutionary dynamics and impact present-day host structure and function, from genome to organism levels. In rare cases, TE community/genome size has greatly expanded in animals, associated with increased cell size and altered anatomy and physiology. We characterize the TE landscape of the genome and transcriptome in an amphibian with a giant genome -- the caecilian Ichthyophis bannanicus, which we show has a genome size of 12.2 Gb. Amphibians are an important model system because the clade includes independent cases of genomic gigantism. The I. bannanicus genome differs compositionally from other giant amphibian genomes, but shares a low rate of ectopic-recombination-mediated deletion. We examine TE activity using expression and divergence plots; TEs account for 15% of somatic transcription, and most superfamilies appear active. We quantify TE diversity in the caecilian, as well as other vertebrates with a range of genome sizes, using diversity indices commonly applied in community ecology. We synthesize previous models integrating TE abundance, diversity, and activity, and we test whether the caecilian meets model predictions for genomes with high TE abundance. We propose thorough, consistent characterization of TEs to strengthen future comparative analyses. Such analyses will ultimately be required to reveal whether the divergent TE assemblages found across convergent gigantic genomes reflect fundamental shared features of TE/host genome evolutionary dynamics.

Size evolution of gigantic genomes suggests stochastic outcomes of transposable element/host silencing interactions

“…In the frogs and non-avian reptiles, TE diversity is higher in smaller genomes, as predicted by several theoretical models (Wang, et al 2021). However, salamanders showed the opposite pattern; TE diversity increases with increasing genome size, in contrast with theoretical predictions.…”

“…We identified transcripts of 22 genes receiving a direct annotation of piRNA processing in vertebrates in the Gene Ontology knowledgebase that were present in the majority of our target species: ASZ1, BTBD18 (BTBDI), DDX4, EXD1, FKBP6, GPAT2, HENMT1 (HENMT), MAEL, MOV10l1 (M10L1), PIWIL1, PIWIL2, PIWIL4, PLD6, PNLDC1 (PNDC1), TDRD1, TDRD5, TDRD6, TDRD7, TDRD9, TDRD12 (TDR12), TDRD15 (TDR15), and TDRKH. In addition, we identified transcripts of 16 genes encoding proteins that create a transcriptionally repressive chromatin environment in response to recruitment by PIWI proteins or KRAB-ZFP proteins, 16 of which received a direct annotation of NuRD complex in the Gene Ontology knowledgebase and 2 of which were taken from the literature: CBX5, CHD3, CHD4, CSNK2A1 , DNMT1, GATAD2A (P66A), HDAC1, MBD3, MTA1, MTA2, MTA3, RBBP4, RBBP7, SALL1, SETDB1 (SETB1), and ZBTB7A (ZBT7A) (Wang, et al 2021)(Ecco et al, 2017. Additionally, we identified TRIM28, which bridges this repressive complex to TE-bound KRAB-ZFP proteins in lobe-finned fishes (Ecco et al, 2017).…”

“…We performed low-coverage genome sequencing, yielding sequencing depths of 0.06X to 0.15X coverage (Supplementary Table S2). Following previous work, we used the PiRATE pipeline which was designed to mine and classify repeats from low-coverage genomic shotgun data in taxa that lack genomic resources (Berthelier, et al 2018;Wang, et al 2021;Wang, et al 2023).…”

“…We selected 88 species of "fishes", frogs, salamanders, non-avian reptiles, birds, and mammals and tested for the predicted negative relationship between TE diversity and genome size in each group (Wang, et al 2021). Diversity of each genomic TE community was measured using both Gini-Simpson's and Shannon diversity indices, considering TE superfamilies as "species" and the percentage of the genome occupied by each TE superfamily as "abundance".…”

Transposable Elements and Stress in Vertebrates: An Overview

“…These retroelements have been found to be really abundant also in the highly repetitive genome of the strawberry poison frog Oophaga pumilio [ 75 ] and have been proposed also as responsible for the gigantism of salamanders [ 73 ]. Instead, the recent analysis performed on the caecilian Ichthyophis bannanicus genome evidenced an abundance of Dictyostelium intermediate repeat sequence (DIRS) and LINE/Jockey elements [ 76 ]. The genomes of non-bird reptiles examined to date showed a TE content ranging from 20% to 30% with a prevalence of LINE retroelements and DNA transposons [ 32 , 77 , 78 , 79 ].…”