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Quantitative Proteomics Reveals Remodeling of Protein Repertoire Across Life Phases of Daphnia pulex.

ABSTRACT: Although the microcrustacean Daphnia is becoming an organism of choice for proteomic studies, protein expression across its life cycle have not been fully characterized. Proteomes of adult females, juveniles, asexually produced embryos, and the ephippia-resting stages containing sexually produced diapausing freezing- and desiccation-resistant embryos are analyzed. Overall, proteins with known molecular functions are more likely to be detected than proteins with no detectable orthology. Similarly, proteins with stronger gene model support in two independent genome assemblies can be detected, than those without such support. This suggests that the proteomics pipeline can be applied to verify hypothesized proteins, even given questionable reference gene models. In particular, upregulation of vitellogenins and downregulation of actins and myosins in embryos of both types, relative to juveniles and adults, and overrepresentation of cell-cycle related proteins in the developing embryos, relative to diapausing embryos and adults, are observed. Upregulation of small heat-shock proteins and peroxidases, as well as overrepresentation of stress-response proteins in the ephippium relative to the asexually produced non-diapausing embryos, is found. The ephippium also shows upregulation of three trehalose-synthesis proteins and downregulation of a trehalose hydrolase, consistent with the role of trehalose in protection against freezing and desiccation.

SUBMITTER: Peshkin L

PROVIDER: S-EPMC7017786 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Quantitative Proteomics Reveals Remodeling of Protein Repertoire Across Life Phases of Daphnia pulex.

Peshkin Leonid L Boukhali Myriam M Haas Wilhelm W Kirschner Marc W MW Yampolsky Lev Y LY

Proteomics 20191210 24

Although the microcrustacean Daphnia is becoming an organism of choice for proteomic studies, protein expression across its life cycle have not been fully characterized. Proteomes of adult females, juveniles, asexually produced embryos, and the ephippia-resting stages containing sexually produced diapausing freezing- and desiccation-resistant embryos are analyzed. Overall, proteins with known molecular functions are more likely to be detected than proteins with no detectable orthology. Similarly ...[more]

PMID: 31697011

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Project description:Long terminal repeat (LTR) retroelements represent a successful group of transposable elements (TEs) that have played an important role in shaping the structure of many eukaryotic genomes. Here, we present a genome-wide analysis of LTR retroelements in Daphnia pulex, a cyclical parthenogen and the first crustacean for which the whole genomic sequence is available. In addition, we analyze transcriptional data and perform transposon display assays of lab-reared lineages and natural isolates to identify potential influences on TE mobility and differences in LTR retroelements loads among individuals reproducing with and without sex.We conducted a comprehensive de novo search for LTR retroelements and identified 333 intact LTR retroelements representing 142 families in the D. pulex genome. While nearly half of the identified LTR retroelements belong to the gypsy group, we also found copia (95), BEL/Pao (66) and DIRS (19) retroelements. Phylogenetic analysis of reverse transcriptase sequences showed that LTR retroelements in the D. pulex genome form many lineages distinct from known families, suggesting that the majority are novel. Our investigation of transcriptional activity of LTR retroelements using tiling array data obtained from three different experimental conditions found that 71 LTR retroelements are actively transcribed. Transposon display assays of mutation-accumulation lines showed evidence for putative somatic insertions for two DIRS retroelement families. Losses of presumably heterozygous insertions were observed in lineages in which selfing occurred, but never in asexuals, highlighting the potential impact of reproductive mode on TE abundance and distribution over time. The same two families were also assayed across natural isolates (both cyclical parthenogens and obligate asexuals) and there were more retroelements in populations capable of reproducing sexually for one of the two families assayed.Given the importance of LTR retroelements activity in the evolution of other genomes, this comprehensive survey provides insight into the potential impact of LTR retroelements on the genome of D. pulex, a cyclically parthenogenetic microcrustacean that has served as an ecological model for over a century.

Project description:BackgroundAcidity exerts a determining influence on the composition and diversity of freshwater faunas. While the physiological implications of freshwater acidification have been intensively studied in teleost fish and crayfish, much less is known about the acid-stress physiology of ecologically important groups such as cladoceran zooplankton. This study analyzed the extracellular acid-base state and CO2 partial pressure (P(CO2)), circulation and ventilation, as well as the respiration rate of Daphnia pulex acclimated to acidic (pH 5.5 and 6.0) and circumneutral (pH 7.8) conditions.ResultsD. pulex had a remarkably high extracellular pH of 8.33 and extracellular P(CO2) of 0.56 kPa under normal ambient conditions (pH 7.8 and normocapnia). The hemolymph had a high bicarbonate concentration of 20.9 mM and a total buffer value of 51.5 meq L(-1) pH(-1). Bicarbonate covered 93% of the total buffer value. Acidic conditions induced a slight acidosis (DeltapH = 0.16-0.23), a 30-65% bicarbonate loss, and elevated systemic activities (tachycardia, hyperventilation, hypermetabolism). pH 6.0 animals partly compensated the bicarbonate loss by increasing the non-bicarbonate buffer value from 2.0 to 5.1 meq L(-1) pH(-1). The extracellular P(CO2) of pH 5.5 animals was significantly reduced to 0.33 kPa, and these animals showed the highest tolerance to a short-term exposure to severe acid stress.ConclusionChronic exposure to acidic conditions had a pervasive impact on Daphnia's physiology including acid-base balance, extracellular PCO2, circulation and ventilation, and energy metabolism. Compensatory changes in extracellular non-bicarbonate buffering capacity and the improved tolerance to severe acid stress indicated the activation of defense mechanisms which may result from gene-expression mediated adjustments in hemolymph buffer proteins and in epithelial properties. Mechanistic analyses of the interdependence between extracellular acid-base balance and CO2 transport raised the question of whether a carbonic anhydrase (CA) is involved in the catalysis of the CO2-HCO3(-)-H(+) reaction, which led to the discovery of 31 CA-genes in the genome of D. pulex.

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Quantitative Proteomics Reveals Remodeling of Protein Repertoire Across Life Phases of Daphnia pulex.

Publications

Quantitative Proteomics Reveals Remodeling of Protein Repertoire Across Life Phases of Daphnia pulex.

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