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DNA evidence for global dispersal and probable endemicity of protozoa.

Bass D, Richards TA, Matthai L, Marsh V, Cavalier-Smith T - BMC Evol. Biol. (2007)

Bottom Line: These results are concordant with the 'moderate endemicity model' of microbial biogeography.Rare or continentally endemic microbes may be ecologically significant and potentially of conservational concern.We also demonstrate that strains with identical 18S but different ITS1 rDNA sequences can differ significantly in terms of morphological and important physiological characteristics, providing strong additional support for global protist biodiversity being significantly higher than previously thought.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, The University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. david.bass@zoo.ox.ac.uk

ABSTRACT

Background: It is much debated whether microbes are easily dispersed globally or whether they, like many macro-organisms, have historical biogeographies. The ubiquitous dispersal hypothesis states that microbes are so numerous and so easily dispersed worldwide that all should be globally distributed and found wherever growing conditions suit them. This has been broadly upheld for protists (microbial eukaryotes) by most morphological and some molecular analyses. However, morphology and most previously used evolutionary markers evolve too slowly to test this important hypothesis adequately.

Results: Here we use a fast-evolving marker (ITS1 rDNA) to map global diversity and distribution of three different clades of cercomonad Protozoa (Eocercomonas and Paracercomonas: phylum Cercozoa) by sequencing multiple environmental gene libraries constructed from 47-80 globally-dispersed samples per group. Even with this enhanced resolution, identical ITS sequences (ITS-types) were retrieved from widely separated sites and on all continents for several genotypes, implying relatively rapid global dispersal. Some identical ITS-types were even recovered from both marine and non-marine samples, habitats that generally harbour significantly different protist communities. Conversely, other ITS-types had either patchy or restricted distributions.

Conclusion: Our results strongly suggest that geographic dispersal in macro-organisms and microbes is not fundamentally different: some taxa show restricted and/or patchy distributions while others are clearly cosmopolitan. These results are concordant with the 'moderate endemicity model' of microbial biogeography. Rare or continentally endemic microbes may be ecologically significant and potentially of conservational concern. We also demonstrate that strains with identical 18S but different ITS1 rDNA sequences can differ significantly in terms of morphological and important physiological characteristics, providing strong additional support for global protist biodiversity being significantly higher than previously thought.

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Phylogeny of cercomonads. BioNJ bootstrap tree (1000 replicates; corrected for Γ & I) of a subset of known cercomonad lineages, representing all known main cercomonad clades and genera (Cercomonas, Eocercomonas, and Paracercomonas) as defined by Karpov et al. [14]. The composition and phylogenetic position of the groups α, β, and γ forming the basis of this study are shown. A group-specific primer set was designed for each of these groups (see Methods).
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Figure 2: Phylogeny of cercomonads. BioNJ bootstrap tree (1000 replicates; corrected for Γ & I) of a subset of known cercomonad lineages, representing all known main cercomonad clades and genera (Cercomonas, Eocercomonas, and Paracercomonas) as defined by Karpov et al. [14]. The composition and phylogenetic position of the groups α, β, and γ forming the basis of this study are shown. A group-specific primer set was designed for each of these groups (see Methods).

Mentions: Cercomonads are benthic heterotrophic flagellates (5–50 μm long) comprising the genera Cercomonas, Eocercomonas, and Paracercomonas [14]. They are abundant in soils [26-28] and aquatic environments, being among the most prominent bacterivorous protozoa. As global dispersal should theoretically be easier for marine protists, making endemicity less likely, we preferentially sampled soil and freshwater environments to test the UDH more rigorously. As some cercomonad 18S-types are globally distributed [10,14], we used ITS1 rDNA sequences, which evolve significantly faster than 18S rDNA sequence (Fig. 1), to determine whether geographically restricted distributions could be detected within cercomonad 18S-types at this higher level of resolution. As there are hundreds of different cercomonad 18S-types [14], we used PCR primers targeted to three very narrow taxonomic groups comprising 1 to 3 18S-types each (Figs 2, 3). This approach enabled us to maximize the chances of detecting the same genotypes in different samples even when rare. To be representative, we targeted three different regions of the cercomonad tree incorporating at least one genus from each of the two main cercomonad clades (Fig. 2) [14]. Our intensive sampling of the rapidly-evolving ITS1 rDNA marker reveals both ubiquitous and restricted distributions and thus demonstrates that biogeography in microbes and macro-organisms differs only in degree. We also show that cercomonad strains within a single 18S-type can differ in terms of phenotype and ecological preferences.


DNA evidence for global dispersal and probable endemicity of protozoa.

Bass D, Richards TA, Matthai L, Marsh V, Cavalier-Smith T - BMC Evol. Biol. (2007)

Phylogeny of cercomonads. BioNJ bootstrap tree (1000 replicates; corrected for Γ & I) of a subset of known cercomonad lineages, representing all known main cercomonad clades and genera (Cercomonas, Eocercomonas, and Paracercomonas) as defined by Karpov et al. [14]. The composition and phylogenetic position of the groups α, β, and γ forming the basis of this study are shown. A group-specific primer set was designed for each of these groups (see Methods).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2194784&req=5

Figure 2: Phylogeny of cercomonads. BioNJ bootstrap tree (1000 replicates; corrected for Γ & I) of a subset of known cercomonad lineages, representing all known main cercomonad clades and genera (Cercomonas, Eocercomonas, and Paracercomonas) as defined by Karpov et al. [14]. The composition and phylogenetic position of the groups α, β, and γ forming the basis of this study are shown. A group-specific primer set was designed for each of these groups (see Methods).
Mentions: Cercomonads are benthic heterotrophic flagellates (5–50 μm long) comprising the genera Cercomonas, Eocercomonas, and Paracercomonas [14]. They are abundant in soils [26-28] and aquatic environments, being among the most prominent bacterivorous protozoa. As global dispersal should theoretically be easier for marine protists, making endemicity less likely, we preferentially sampled soil and freshwater environments to test the UDH more rigorously. As some cercomonad 18S-types are globally distributed [10,14], we used ITS1 rDNA sequences, which evolve significantly faster than 18S rDNA sequence (Fig. 1), to determine whether geographically restricted distributions could be detected within cercomonad 18S-types at this higher level of resolution. As there are hundreds of different cercomonad 18S-types [14], we used PCR primers targeted to three very narrow taxonomic groups comprising 1 to 3 18S-types each (Figs 2, 3). This approach enabled us to maximize the chances of detecting the same genotypes in different samples even when rare. To be representative, we targeted three different regions of the cercomonad tree incorporating at least one genus from each of the two main cercomonad clades (Fig. 2) [14]. Our intensive sampling of the rapidly-evolving ITS1 rDNA marker reveals both ubiquitous and restricted distributions and thus demonstrates that biogeography in microbes and macro-organisms differs only in degree. We also show that cercomonad strains within a single 18S-type can differ in terms of phenotype and ecological preferences.

Bottom Line: These results are concordant with the 'moderate endemicity model' of microbial biogeography.Rare or continentally endemic microbes may be ecologically significant and potentially of conservational concern.We also demonstrate that strains with identical 18S but different ITS1 rDNA sequences can differ significantly in terms of morphological and important physiological characteristics, providing strong additional support for global protist biodiversity being significantly higher than previously thought.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, The University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. david.bass@zoo.ox.ac.uk

ABSTRACT

Background: It is much debated whether microbes are easily dispersed globally or whether they, like many macro-organisms, have historical biogeographies. The ubiquitous dispersal hypothesis states that microbes are so numerous and so easily dispersed worldwide that all should be globally distributed and found wherever growing conditions suit them. This has been broadly upheld for protists (microbial eukaryotes) by most morphological and some molecular analyses. However, morphology and most previously used evolutionary markers evolve too slowly to test this important hypothesis adequately.

Results: Here we use a fast-evolving marker (ITS1 rDNA) to map global diversity and distribution of three different clades of cercomonad Protozoa (Eocercomonas and Paracercomonas: phylum Cercozoa) by sequencing multiple environmental gene libraries constructed from 47-80 globally-dispersed samples per group. Even with this enhanced resolution, identical ITS sequences (ITS-types) were retrieved from widely separated sites and on all continents for several genotypes, implying relatively rapid global dispersal. Some identical ITS-types were even recovered from both marine and non-marine samples, habitats that generally harbour significantly different protist communities. Conversely, other ITS-types had either patchy or restricted distributions.

Conclusion: Our results strongly suggest that geographic dispersal in macro-organisms and microbes is not fundamentally different: some taxa show restricted and/or patchy distributions while others are clearly cosmopolitan. These results are concordant with the 'moderate endemicity model' of microbial biogeography. Rare or continentally endemic microbes may be ecologically significant and potentially of conservational concern. We also demonstrate that strains with identical 18S but different ITS1 rDNA sequences can differ significantly in terms of morphological and important physiological characteristics, providing strong additional support for global protist biodiversity being significantly higher than previously thought.

Show MeSH
Related in: MedlinePlus