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Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life.

ABSTRACT: BACKGROUND:Transitions from marine to intertidal and terrestrial habitats resulted in a significant adaptive radiation within the Panpulmonata (Gastropoda: Heterobranchia). This clade comprises several groups that invaded the land realm independently and in different time periods, e.g., Ellobioidea, Systellomatophora, and Stylommatophora. Thus, mitochondrial genomes of panpulmonate gastropods are promising to screen for adaptive molecular signatures related to land invasions. RESULTS:We obtained three complete mitochondrial genomes of terrestrial panpulmonates, i.e., the ellobiid Carychium tridentatum, and the stylommatophorans Arion rufus and Helicella itala. Our dataset consisted of 50 mitogenomes comprising almost all major panpulmonate lineages. The phylogenetic tree based on mitochondrial genes supports the monophyly of the clade Panpulmonata. Terrestrial lineages were sampled from Ellobioidea (1 sp.) and Stylommatophora (9 spp.). The branch-site test of positive selection detected significant non-synonymous changes in the terrestrial branches leading to Carychium (Ellobiodea) and Stylommatophora. These convergent changes occurred in the cob and nad5 genes (OXPHOS complex III and I, respectively). CONCLUSIONS:The convergence of the non-synonymous changes in cob and nad5 suggest possible ancient episodes of positive selection related to adaptations to non-marine habitats. The positively selected sites in our data are in agreement with previous results in vertebrates suggesting a general pattern of adaptation to the new metabolic requirements. The demand for energy due to the colonization of land (for example, to move and sustain the body mass in the new habitat) and the necessity to tolerate new conditions of abiotic stress may have changed the physiological constraints in the early terrestrial panpulmonates and triggered adaptations at the mitochondrial level.

SUBMITTER: Romero PE

PROVIDER: S-EPMC4994307 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life.

Romero Pedro E PE Weigand Alexander M AM Pfenninger Markus M

BMC evolutionary biology 20160822 1

<h4>Background</h4>Transitions from marine to intertidal and terrestrial habitats resulted in a significant adaptive radiation within the Panpulmonata (Gastropoda: Heterobranchia). This clade comprises several groups that invaded the land realm independently and in different time periods, e.g., Ellobioidea, Systellomatophora, and Stylommatophora. Thus, mitochondrial genomes of panpulmonate gastropods are promising to screen for adaptive molecular signatures related to land invasions.<h4>Results< ...[more]

PMID: 27549326

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Project description:We examined the genomic adaptations of prevalent bacterial taxa in a highly nutrient- and ion-depleted freshwater environment located in the secondary cooling water system of a nuclear research reactor. Using genome-centric metagenomics, we found that none of the prevalent bacterial taxa were related to typical freshwater bacterial lineages. We also did not identify strong signatures of genome streamlining, which has been shown to be one of the ecoevolutionary forces shaping the genome characteristics of bacterial taxa in nutrient-depleted environments. Instead, focusing on the dominant taxon, a novel Ramlibacter sp. which we propose to name Ramlibacter aquaticus, we detected extensive positive selection on genes involved in phosphorus and carbon scavenging pathways. These genes were involved in the high-affinity phosphate uptake and storage into polyphosphate granules, metabolism of nitrogen-rich organic matter, and carbon/energy storage into polyhydroxyalkanoate. In parallel, comparative genomics revealed a high number of paralogs and an accessory genome significantly enriched in environmental sensing pathways (i.e., chemotaxis and motility), suggesting extensive gene expansions in R. aquaticus The type strain of R. aquaticus (LMG 30558T) displayed optimal growth kinetics and productivity at low nutrient concentrations, as well as substantial cell size plasticity. Our findings with R. aquaticus LMG 30558T demonstrate that positive selection and gene expansions may represent successful adaptive strategies to oligotrophic environments that preserve high growth rates and cellular productivity.IMPORTANCE By combining a genome-centric metagenomic approach with a culture-based approach, we investigated the genomic adaptations of prevalent populations in an engineered oligotrophic freshwater system. We found evidence for widespread positive selection on genes involved in phosphorus and carbon scavenging pathways and for gene expansions in motility and environmental sensing to be important genomic adaptations of the abundant taxon in this system. In addition, microscopic and flow cytometric analysis of the first freshwater representative of this population (Ramlibacter aquaticus LMG 30558T) demonstrated phenotypic plasticity, possibly due to the metabolic versatility granted by its larger genome, to be a strategy to cope with nutrient limitation. Our study clearly demonstrates the need for the use of a broad set of genomic tools combined with culture-based physiological characterization assays to investigate and validate genomic adaptations.

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Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life.

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Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life.

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