Gene Family Evolution Reflects Adaptation to Soil Environmental Stressors in the Genome of the CollembolanOrchesella cincta

Abstract

Collembola (springtails) are detritivorous hexapods that inhabit the soil and its litter layer. The ecology of the springtail Orchesella cincta is extensively studied in the context of adaptation to anthropogenically disturbed areas. Here, we present a draft genome of an O. cincta reference strain with an estimated size of 286.8 Mbp, containing 20,249 genes. In total, 446 gene families are expanded and 1,169 gene families evolved specific to this lineage. Besides these gene families involved in general biological processes, we observe gene clusters participating in xenobiotic biotransformation. Furthermore, we identified 253 cases of horizontal gene transfer (HGT). Although the largest percentage of them originated from bacteria (37.5%), we observe an unusually high percentage (30.4%) of such genes of fungal origin. The majority of foreign genes are involved in carbohydrate metabolism and cellulose degradation. Moreover, some foreign genes (e.g., bacillopeptidases) expanded after HGT. We hypothesize that horizontally transferred genes could be advantageous for food processing in a soil environment that is full of decaying organic material. Finally, we identified several lineage-specific genes, expanded gene families, and horizontally transferred genes, associated with altered gene expression as a consequence of genetic adaptation to metal stress. This suggests that these genome features may be preadaptations allowing natural selection to act on. In conclusion, this genome study provides a solid foundation for further analysis of evolutionary mechanisms of adaptation to environmental stressors.

Evolutionary ecology of beta‐lactam gene clusters in animals

“…Furthermore, evidence for extensive horizontal gene transfer from fungi to the springtail Orchesella cincta has been reported (Faddeeva‐Vakhrusheva et al . ).…”

“…5) and many springtails feed on fungi or fall prey to insectivorous fungi. Furthermore, evidence for extensive horizontal gene transfer from fungi to the springtail Orchesella cincta has been reported (Faddeeva-Vakhrusheva et al 2016).…”

“…Based on this robust procedure, we identified between 1.2% and 2.8% of HGT genes in two Collembolan genomes (Faddeeva‐Vakhrusheva et al . ).…”

“…In fact, Crisp et al (2015) developed a method to systematically detect HGT in a genome-wide context, including BLAST information, phylogeny and a physical genome linkage test (Crisp et al 2015). Based on this robust procedure, we identified between 1.2% and 2.8% of HGT genes in two Collembolan genomes (Faddeeva-Vakhrusheva et al 2016).…”

At the confluence of vicariance and dispersal: Phylogeography of cavernicolous springtails (Collembola: Arrhopalitidae, Tomoceridae) codistributed across a geologically complex karst landscape in Illinois and Missouri

“…Their great abundance, low vagility, long‐term local persistence, and remarkable ecological specificity renders springtails excellent sources of information for inferring biogeographic processes (Garrick, Rowell, Simmons, Hillis, & Sunnucks, ). However, there are both technical and practical limitations to their use for biogeography, including but not restricted to (a) low single‐specimen DNA yields via modern extraction methodologies hinders opportunities for population‐level genomic‐scale analyses; (b) rampant cryptic speciation throughout Class Collembola, renders a priori taxonomic sampling for DNA extraction difficult, if not impossible; (c) limited taxonomic and gene coverage of available reference sequences—genomic datasets have only recently become available for three species (Faddeeva‐Vakhrusheva et al., , ; Wu et al., ); and (d) the dearth of financial resources devoted to springtail research despite their ecological and evolutionary importance. These limitations are reflected in the small molecular datasets (relative to modern genomic standards) and reliance of mitochondrial markers for springtail phylogeography.…”