Dataset Information

Gene Family Evolution Reflects Adaptation to Soil Environmental Stressors in the Genome of the Collembolan Orchesella 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.

SUBMITTER: Faddeeva-Vakhrusheva A

PROVIDER: S-EPMC4987106 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Gene Family Evolution Reflects Adaptation to Soil Environmental Stressors in the Genome of the Collembolan Orchesella cincta.

Faddeeva-Vakhrusheva Anna A Derks Martijn F L MF Anvar Seyed Yahya SY Agamennone Valeria V Suring Wouter W Smit Sandra S van Straalen Nico M NM Roelofs Dick D

Genome biology and evolution 20160712 7

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 ...[more]

PMID: 27289101

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Project description:Field-selected tolerance to heavy metals has been reported for Orchesella cincta (Arthropoda: Collembola) populations occurring at metal-contaminated mining sites. This tolerance is correlated with heritable increase of metal excretion efficiency; less pronounce cadmium induced growth reduction and, over-expression of the metallothionein gene. We applied transcriptomics to determine differential gene expression caused by this abiotic stress in reference and cadmium tolerant populations. Many cDNAs responded to cadmium exposure in a reference population. Significantly fewer clones were cadmium responsive in tolerant animals. Analysis of variance revealed transcripts that interact between cadmium exposure and population. Hierarchical clustering of these clones revealed two major groups. The first one contained cDNAs that were up regulated by cadmium in the reference culture, but non-responsive or down regulated in tolerant animals. This cluster was also characterized by elevated constitutive expression in the tolerant population. Gene ontology analysis revealed that these cDNAs were involved in structural integrity of the cuticle, anti-microbial defense, calcium-channel blocking, neurotransmitter transport, chromatin remodeling and, endoplasmatic vesicle activity. The second group consisted of cDNAs down regulated in reference animals but not responding or slightly up regulated in tolerant animals. Their functions involved carbohydrate metabolic processes, Ca2+ dependent stress signaling, proteolysis and digestion. The reference population showed a strong signature of stress-induced genome-wide perturbation of gene expression, whereas the tolerant animals maintained normal gene expression upon cadmium exposure. We confirmed the micro-evolutionary processes occurring in soil arthropod populations and suggest a major contribution of gene regulation to the evolution of a stress-adapted phenotype. Orchesella cincta (Collembola) from the laboratory population (LC) at the department of Animal Ecology, Vrije Universiteit Amsterdam were taken as the reference group. This population originated from a pine forest from the reference area (Roggebotzand, the Netherlands, latitude N = 52 º 34’17’’, longitude E = 5 º 47’56’’) that contains on average < 0.5 μg cadmium per gram litter and humus. Tolerant animals were collected from randomly selected litter samples at two areas of the abandoned, but still heavily polluted lead/zinc mining site of Plombières (Belgium, latitude N = 50˚44’03’’, longitude E = 5˚58’02’’): the locations contain an average cadmium concentration between 10 and 52 μg.g-1 soil (Lock et al. 2003; Sterenborg 2003; Van Straalen et al. 1987). To diminish putative environmental effects from the field the animals were reared in a climate room (20°C, 75% humidity, LD 12 h:12 h) in PVC jars on a moist plaster of Paris layer feeding on algae present on twigs for at least three generations before experimental treatment. Animals were exposed to cadmium (nominal concentration of 112,4 μg cadmium.g-1 dry algae) for 3 days, directly after molting, via algal food. Control groups received the same treatment except that water was spiked into the algal food instead of cadmium solution. The cadmium exposure concentration is two times the no observed effect concentration (NOEC) for reproduction in chronically exposed animals. Total RNA was extracted from times 12 pooled animals per treatment using SV Total RNA Isolation system (Promega) and quantified on a Nanodrop ND-1000 Spectrophotometer (Nanodrop Technologies). Total RNA was visualized on a 1.5% agarose gel to verify its integrity. Each experimental group (pool of 12 animals) was replicated 8 times. Dyes were swapped between biological replicates: 4 Cy-3 labeled replicates and 4 Cy-5 lebeled replicates per experimental group Microarray experiment was designed in a closed loop Lab culture clean vs Cd, Lab culture Cd vs Tolerant culture Cd, Tolerant culture Cd vs Tolerant culture clean, Tolerant culture clean vs lab culture clean

Dataset Information

Gene Family Evolution Reflects Adaptation to Soil Environmental Stressors in the Genome of the Collembolan Orchesella cincta.

Publications

Gene Family Evolution Reflects Adaptation to Soil Environmental Stressors in the Genome of the Collembolan Orchesella cincta.

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