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Evolution of the actin gene family in testate lobose amoebae (Arcellinida) is characterized by two distinct clades of paralogs and recent independent expansions.

ABSTRACT: The evolution of actin gene families is characterized by independent expansions and contractions across the eukaryotic tree of life. Here, we assess diversity of actin gene sequences within three lineages of the genus Arcella, a free-living testate (shelled) amoeba in the Arcellinida. We established four clonal lines of two morphospecies, Arcella hemisphaerica and A. vulgaris, and assessed their phylogenetic relationship within the "Amoebozoa" using small subunit ribosomal DNA (SSU-rDNA) genealogy. We determined that the two lines of A. hemisphaerica are identical in SSU-rDNA, while the two A. vulgaris are independent genetic lineages. Furthermore, we characterized multiple actin gene copies from all lineages. Analyses of the resulting sequences reveal numerous diverse actin genes, which differ mostly by synonymous substitutions. We estimate that the actin gene family contains 40-50 paralogous members in each lineage. None of the three independent lineages share the same paralog with another, and divergence between actins reaches 29% in contrast to just 2% in SSU-rDNA. Analyses of effective number of codons (ENC), compositional bias, recombination signatures, and genetic diversity in the context of a gene tree indicate that there are two groups of actins evolving with distinct patterns of molecular evolution. Within these groups, there have been multiple independent expansions of actin genes within each lineage. Together, these data suggest that the two groups are located in different regions of the Arcella genome. Furthermore, we compare the Arcella actin gene family with the relatively well-described gene family in the slime mold Dictyostelium discoideum and other members of the Amoebozoa clade. Overall patterns of molecular evolution are similar in Arcella and Dictyostelium. However, the separation of genes in two distinct groups coupled with recent expansion is characteristic of Arcella and might reflect an unusual pattern of gene family evolution in the lobose testate amoebae. We provide a model to account for both the existence of two distinct groups and the pattern of recent independent expansion leading to a large number of actins in each lineage.

SUBMITTER: Lahr DJ

PROVIDER: S-EPMC3108602 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Evolution of the actin gene family in testate lobose amoebae (Arcellinida) is characterized by two distinct clades of paralogs and recent independent expansions.

Lahr Daniel J G DJ Nguyen Truc B TB Barbero Erika E Katz Laura A LA

Molecular biology and evolution 20100802 1

The evolution of actin gene families is characterized by independent expansions and contractions across the eukaryotic tree of life. Here, we assess diversity of actin gene sequences within three lineages of the genus Arcella, a free-living testate (shelled) amoeba in the Arcellinida. We established four clonal lines of two morphospecies, Arcella hemisphaerica and A. vulgaris, and assessed their phylogenetic relationship within the "Amoebozoa" using small subunit ribosomal DNA (SSU-rDNA) genealo ...[more]

PMID: 20679092

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Project description:Arcellinida (testate lobose amoebae) were examined from 40 near-surface sediment samples (top 0.5 cm) from two lakes impacted by arsenic (As) contamination associated with legacy gold mining in subarctic Canada. The objectives of the study are two folds: quantify the response of Arcellinida to intra-lake variability of As and other physicochemical controls, and evaluate whether the impact of As contamination derived from two former gold mines, Giant Mine (1938-2004) and Tundra Mine (1964-1968 and 1983-1986), on the Arcellinida distribution in both lakes is comparable or different. Cluster analysis and nonmetric multidimensional scaling (NMDS) were used to identify Arcellinida assemblages in both lakes, and redundancy analysis (RDA) was used to quantify the relationship between the assemblages, As, and other geochemical and sedimentological parameters. Cluster analysis and NMDS revealed four distinct arcellinidan assemblages in Frame Lake (assemblages 1-4) and two in Hambone Lake (assemblages 5 and 6): (1) Extreme As Contamination (EAC) Assemblage; (2) High calcium (HC) Assemblage; (3) Moderate As Contamination (MAC) assemblages; (4) High Nutrients (HN) Assemblage; (5) High Diversity (HD) Assemblage; and (6) Centropyxis aculeata (CA) Assemblage. RDA analysis showed that the faunal structure of the Frame Lake assemblages was controlled by five variables that explained 43.2% of the total faunal variance, with As (15.8%), Olsen phosphorous (Olsen-P; 10.5%), and Ca (9.5%) being the most statistically significant (p < 0.004). Stress-tolerant arcellinidan taxa were associated with elevated As concentrations (e.g., EAC and MAC; As concentrations range = 145.1-1336.6 mg kg-1; n = 11 samples), while stress-sensitive taxa thrived in relatively healthier assemblages found in substrates with lower As concentrations and higher concentrations of nutrients, such as Olsen-P and Ca (e.g., HC and HM; As concentrations range = 151.1-492.3 mg kg-1; n = 14 samples). In contrast, the impact of As on the arcellinidan distribution was not statistically significant in Hambone Lake (7.6%; p-value = 0.152), where the proportion of silt (24.4%; p-value = 0.005) and loss-on-ignition-determined minerogenic content (18.5%; p-value = 0.021) explained a higher proportion of the total faunal variance (58.4%). However, a notable decrease in arcellinidan species richness and abundance and increase in the proportions of stress-tolerant fauna near Hambone Lake's outlet (e.g., CA samples) is consistent with a spatial gradient of higher sedimentary As concentration near the outlet, and suggests a lasting, albeit weak, As influence on Arcellinida distribution in the lake. We interpret differences in the influence of sedimentary As concentration on Arcellinida to differences in the predominant As mineralogy in each lake, which is in turn influenced by differences in ore-processing at the former Giant (roasting) and Tundra mines (free-milling).

Project description:Peatland testate amoebae (TA) are well-established bioindicators for depth to water table (DWT), but effects of hydrological changes on TA communities have never been tested experimentally. We tested this in a field experiment by placing Sphagnum carpets (15 cm diameter) collected in hummock, lawn and pool microsites (origin) at three local conditions (dry, moist and wet) using trenches dug in a peatland. One series of samples was seeded with microorganism extract from all microsites. TA community were analysed at T0: 8-2008, T1: 5-2009 and T2: 8-2009. We analysed the data using conditional inference trees, principal response curves (PRC) and DWT inferred from TA communities using a transfer function used for paleoecological reconstruction. Density declined from T0 to T1 and then increased sharply by T2. Species richness, Simpson diversity and Simpson evenness were lower at T2 than at T0 and T1. Seeded communities had higher species richness in pool samples at T0. Pool samples tended to have higher density, lower species richness, Simpson diversity and Simpson Evenness than hummock and/or lawn samples until T1. In the PRC, the effect of origin was significant at T0 and T1, but the effect faded away by T2. Seeding effect was strongest at T1 and lowest vanished by T2. Local condition effect was strong but not in line with the wetness gradient at T1 but started to reflect it by T2. Likewise, TA-inferred DWT started to match the experimental conditions by T2, but more so in hummock and lawn samples than in pool samples. This study confirmed that TA responds to hydrological changes over a 1-year period. However, sensitivity of TA to hydrological fluctuations, and thus the accuracy of inferred DWT changes, was habitat specific, pool TA communities being least responsive to environmental changes. Lawns and hummocks may be thus better suited than pools for paleoecological reconstructions. This, however, contrasts with the higher prediction error and species' tolerance for DWT with increasing dryness observed in transfer function models.

Dataset Information

Evolution of the actin gene family in testate lobose amoebae (Arcellinida) is characterized by two distinct clades of paralogs and recent independent expansions.

Publications

Evolution of the actin gene family in testate lobose amoebae (Arcellinida) is characterized by two distinct clades of paralogs and recent independent expansions.

Similar Datasets

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