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DNA-Based Taxonomy in Ecologically Versatile Microalgae: A Re-Evaluation of the Species Concept within the Coccoid Green Algal Genus Coccomyxa (Trebouxiophyceae, Chlorophyta).

Malavasi V, Škaloud P, Rindi F, Tempesta S, Paoletti M, Pasqualetti M - PLoS ONE (2016)

Bottom Line: Our results are compared with those of a recent integrative study of Darienko and colleagues that reassessed the taxonomy of Coccomyxa, recognizing 7 species in the genus.We conclude that the 27-species scenario is presently the most realistic for Coccomyxa and we suggest that well-supported lineages distinguishable by ecological preferences should be recognized as different species in this genus.We also recommend that for microbial lineages in which the overall diversity is unknown and taxon sampling is sparse, as is often the case for green microalgae, the results of analyses for algorithmic DNA-based species delimitation should be interpreted with extreme caution.

View Article: PubMed Central - PubMed

Affiliation: Interdepartmental Center of Environmental Science and Engineering (CINSA), University of Cagliari, Cagliari, Italy.

ABSTRACT
Coccomyxa is a genus of unicellular green algae of the class Trebouxiophyceae, well known for its cosmopolitan distribution and great ecological amplitude. The taxonomy of this genus has long been problematic, due to reliance on badly-defined and environmentally variable morphological characters. In this study, based on the discovery of a new species from an extreme habitat, we reassess species circumscription in Coccomyxa, a unicellular genus of the class Trebouxiophyceae, using a combination of ecological and DNA sequence data (analyzed with three different methods of algorithmic species delineation). Our results are compared with those of a recent integrative study of Darienko and colleagues that reassessed the taxonomy of Coccomyxa, recognizing 7 species in the genus. Expanding the dataset from 43 to 61 sequences (SSU + ITS rDNA) resulted in a different delimitation, supporting the recognition of a higher number of species (24 to 27 depending on the analysis used, with the 27-species scenario receiving the strongest support). Among these, C. melkonianii sp. nov. is described from material isolated from a river highly polluted by heavy metals (Rio Irvi, Sardinia, Italy). Analyses performed on ecological characters detected a significant phylogenetic signal in six different characters. We conclude that the 27-species scenario is presently the most realistic for Coccomyxa and we suggest that well-supported lineages distinguishable by ecological preferences should be recognized as different species in this genus. We also recommend that for microbial lineages in which the overall diversity is unknown and taxon sampling is sparse, as is often the case for green microalgae, the results of analyses for algorithmic DNA-based species delimitation should be interpreted with extreme caution.

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Estimated evolution of ecological traits within the genus Coccomyxa.Ancestral reconstructions of the living stage (A) and habitat ecological characteristics (B) were inferred using the ACCTRAN parsimony method. The topologies shown were obtained by BEAST analyses based on a concatenated SSU + ITS rDNA dataset, using alignments reduced to include only well-aligned ITS positions. Circles at terminal nodes represent the observed trait state for extant species. Pie charts for ancestral nodes show estimated proportions for reconstructed trait states at that internal node. Different species scenarios proposed by GMYC and bPTP analyses are indicated by vertical bars next to the phylogenetic trees. Clade colouring and labelling follows the Figs 4 and 5.
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pone.0151137.g006: Estimated evolution of ecological traits within the genus Coccomyxa.Ancestral reconstructions of the living stage (A) and habitat ecological characteristics (B) were inferred using the ACCTRAN parsimony method. The topologies shown were obtained by BEAST analyses based on a concatenated SSU + ITS rDNA dataset, using alignments reduced to include only well-aligned ITS positions. Circles at terminal nodes represent the observed trait state for extant species. Pie charts for ancestral nodes show estimated proportions for reconstructed trait states at that internal node. Different species scenarios proposed by GMYC and bPTP analyses are indicated by vertical bars next to the phylogenetic trees. Clade colouring and labelling follows the Figs 4 and 5.

Mentions: Summarizing our results, statistical tests showed narrowly defined species to be significantly better delimited by their ecology than the broadly delimited species, indicating the 27-species scenario to be the most consistent with ecological data. Indeed, a number of narrowly defined species can be well characterized by various ecological traits (Fig 6). Differences in living stage can be well applied to delimit species within the C. simplex s.l. (Fig 6A): C. solorinae and clade A represent lichen photobionts, whereas C. elongata and clade B include free living strains only. In addition, C. simplex s.str. and clade D comprise free-living species often entering into symbiotic association with the heterotrophic ciliates. Further ecological differentiation of narrowly defined species can be revealed when considering habitat-related traits (Fig 6B). For example, the terrestrial strains generally clustered in C. galuniae and the clade E. However, whereas the former species can be also found in aquatic environment, the latter one is strictly aerophytic. Within C. simplex s.l., the association with an extreme environment (a river with very high contents of heavy metals) was exclusive of Coccomyxa SCCA048, hereafter described as Coccomyxa melkonianii sp. nov.


DNA-Based Taxonomy in Ecologically Versatile Microalgae: A Re-Evaluation of the Species Concept within the Coccoid Green Algal Genus Coccomyxa (Trebouxiophyceae, Chlorophyta).

Malavasi V, Škaloud P, Rindi F, Tempesta S, Paoletti M, Pasqualetti M - PLoS ONE (2016)

Estimated evolution of ecological traits within the genus Coccomyxa.Ancestral reconstructions of the living stage (A) and habitat ecological characteristics (B) were inferred using the ACCTRAN parsimony method. The topologies shown were obtained by BEAST analyses based on a concatenated SSU + ITS rDNA dataset, using alignments reduced to include only well-aligned ITS positions. Circles at terminal nodes represent the observed trait state for extant species. Pie charts for ancestral nodes show estimated proportions for reconstructed trait states at that internal node. Different species scenarios proposed by GMYC and bPTP analyses are indicated by vertical bars next to the phylogenetic trees. Clade colouring and labelling follows the Figs 4 and 5.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814044&req=5

pone.0151137.g006: Estimated evolution of ecological traits within the genus Coccomyxa.Ancestral reconstructions of the living stage (A) and habitat ecological characteristics (B) were inferred using the ACCTRAN parsimony method. The topologies shown were obtained by BEAST analyses based on a concatenated SSU + ITS rDNA dataset, using alignments reduced to include only well-aligned ITS positions. Circles at terminal nodes represent the observed trait state for extant species. Pie charts for ancestral nodes show estimated proportions for reconstructed trait states at that internal node. Different species scenarios proposed by GMYC and bPTP analyses are indicated by vertical bars next to the phylogenetic trees. Clade colouring and labelling follows the Figs 4 and 5.
Mentions: Summarizing our results, statistical tests showed narrowly defined species to be significantly better delimited by their ecology than the broadly delimited species, indicating the 27-species scenario to be the most consistent with ecological data. Indeed, a number of narrowly defined species can be well characterized by various ecological traits (Fig 6). Differences in living stage can be well applied to delimit species within the C. simplex s.l. (Fig 6A): C. solorinae and clade A represent lichen photobionts, whereas C. elongata and clade B include free living strains only. In addition, C. simplex s.str. and clade D comprise free-living species often entering into symbiotic association with the heterotrophic ciliates. Further ecological differentiation of narrowly defined species can be revealed when considering habitat-related traits (Fig 6B). For example, the terrestrial strains generally clustered in C. galuniae and the clade E. However, whereas the former species can be also found in aquatic environment, the latter one is strictly aerophytic. Within C. simplex s.l., the association with an extreme environment (a river with very high contents of heavy metals) was exclusive of Coccomyxa SCCA048, hereafter described as Coccomyxa melkonianii sp. nov.

Bottom Line: Our results are compared with those of a recent integrative study of Darienko and colleagues that reassessed the taxonomy of Coccomyxa, recognizing 7 species in the genus.We conclude that the 27-species scenario is presently the most realistic for Coccomyxa and we suggest that well-supported lineages distinguishable by ecological preferences should be recognized as different species in this genus.We also recommend that for microbial lineages in which the overall diversity is unknown and taxon sampling is sparse, as is often the case for green microalgae, the results of analyses for algorithmic DNA-based species delimitation should be interpreted with extreme caution.

View Article: PubMed Central - PubMed

Affiliation: Interdepartmental Center of Environmental Science and Engineering (CINSA), University of Cagliari, Cagliari, Italy.

ABSTRACT
Coccomyxa is a genus of unicellular green algae of the class Trebouxiophyceae, well known for its cosmopolitan distribution and great ecological amplitude. The taxonomy of this genus has long been problematic, due to reliance on badly-defined and environmentally variable morphological characters. In this study, based on the discovery of a new species from an extreme habitat, we reassess species circumscription in Coccomyxa, a unicellular genus of the class Trebouxiophyceae, using a combination of ecological and DNA sequence data (analyzed with three different methods of algorithmic species delineation). Our results are compared with those of a recent integrative study of Darienko and colleagues that reassessed the taxonomy of Coccomyxa, recognizing 7 species in the genus. Expanding the dataset from 43 to 61 sequences (SSU + ITS rDNA) resulted in a different delimitation, supporting the recognition of a higher number of species (24 to 27 depending on the analysis used, with the 27-species scenario receiving the strongest support). Among these, C. melkonianii sp. nov. is described from material isolated from a river highly polluted by heavy metals (Rio Irvi, Sardinia, Italy). Analyses performed on ecological characters detected a significant phylogenetic signal in six different characters. We conclude that the 27-species scenario is presently the most realistic for Coccomyxa and we suggest that well-supported lineages distinguishable by ecological preferences should be recognized as different species in this genus. We also recommend that for microbial lineages in which the overall diversity is unknown and taxon sampling is sparse, as is often the case for green microalgae, the results of analyses for algorithmic DNA-based species delimitation should be interpreted with extreme caution.

Show MeSH