Limits...
Some considerations for analyzing biodiversity using integrative metagenomics and gene networks.

Bittner L, Halary S, Payri C, Cruaud C, de Reviers B, Lopez P, Bapteste E - Biol. Direct (2010)

Bottom Line: We reached these conclusions through a comparison of the theoretical foundations of two molecular approaches seeking to assess biodiversity: metagenomics (mostly used on prokaryotes and protists) and DNA barcoding (mostly used on multicellular eukaryotes), and by pragmatic considerations of the issues caused by the 'species problem' in biodiversity studies.Evolutionary gene networks reduce the risk of producing biodiversity estimates with limited explanatory power, biased either by unequal rates of LGT, or difficult to interpret due to (practical) problems caused by type I and type II grey zones.Moreover, these networks would easily accommodate additional (meta)transcriptomic and (meta)proteomic data.

View Article: PubMed Central - HTML - PubMed

Affiliation: UMR CNRS 7138 Systématique, Adaptation, Evolution, Université Pierre et Marie Curie, Paris, France.

ABSTRACT

Background: Improving knowledge of biodiversity will benefit conservation biology, enhance bioremediation studies, and could lead to new medical treatments. However there is no standard approach to estimate and to compare the diversity of different environments, or to study its past, and possibly, future evolution.

Presentation of the hypothesis: We argue that there are two conditions for significant progress in the identification and quantification of biodiversity. First, integrative metagenomic studies - aiming at the simultaneous examination (or even better at the integration) of observations about the elements, functions and evolutionary processes captured by the massive sequencing of multiple markers - should be preferred over DNA barcoding projects and over metagenomic projects based on a single marker. Second, such metagenomic data should be studied with novel inclusive network-based approaches, designed to draw inferences both on the many units and on the many processes present in the environments.

Testing the hypothesis: We reached these conclusions through a comparison of the theoretical foundations of two molecular approaches seeking to assess biodiversity: metagenomics (mostly used on prokaryotes and protists) and DNA barcoding (mostly used on multicellular eukaryotes), and by pragmatic considerations of the issues caused by the 'species problem' in biodiversity studies.

Implications of the hypothesis: Evolutionary gene networks reduce the risk of producing biodiversity estimates with limited explanatory power, biased either by unequal rates of LGT, or difficult to interpret due to (practical) problems caused by type I and type II grey zones. Moreover, these networks would easily accommodate additional (meta)transcriptomic and (meta)proteomic data.

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Four remarkable situations when distinct species concepts are applied. Each species concept groups a set of organisms, as members of a species taxon, as illustrated by a colored circle (purple for the phylogenetic species, green for the recombining or biological species, blue for the morphological species, pink for the barcode-based species). The overlap between groups is indicated by red dashes. A. In prokaryotes, the groups defined by the various species concepts are largely not nested. A unified species concept would be a poor descriptor of biodiversity: inter-approach pluralism is an issue for species definition. So is intra-approach pluralism, as indicated by smaller circles corresponding to the incongruent groups proposed by different markers, for a given species concept. B. Exploratory use of DNA barcoding to define groups of specimens belonging to a same species. On a histogram of p-distances frequencies, the identification of a barcode gap provides a threshold over which two specimens cannot belong to the same species. The monophyly of specimens falling in a same group can also be assessed. C. The ideal case: all the species concepts identify the same sets of organisms. Intra- and inter-approach pluralisms are not a problem. A unified species concept is a good descriptor of biodiversity D. Type I grey zone: the species concepts produce a series of nested groups. Ranking these groups is an issue. E. Type II grey zone: the species concepts produce partially non-nested groups. Inter- and intra-approach pluralism can be problematic. For cases D & E, pragmatic descriptors would be more accurate and informative about biodiversity than a unified species concept.
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Figure 1: Four remarkable situations when distinct species concepts are applied. Each species concept groups a set of organisms, as members of a species taxon, as illustrated by a colored circle (purple for the phylogenetic species, green for the recombining or biological species, blue for the morphological species, pink for the barcode-based species). The overlap between groups is indicated by red dashes. A. In prokaryotes, the groups defined by the various species concepts are largely not nested. A unified species concept would be a poor descriptor of biodiversity: inter-approach pluralism is an issue for species definition. So is intra-approach pluralism, as indicated by smaller circles corresponding to the incongruent groups proposed by different markers, for a given species concept. B. Exploratory use of DNA barcoding to define groups of specimens belonging to a same species. On a histogram of p-distances frequencies, the identification of a barcode gap provides a threshold over which two specimens cannot belong to the same species. The monophyly of specimens falling in a same group can also be assessed. C. The ideal case: all the species concepts identify the same sets of organisms. Intra- and inter-approach pluralisms are not a problem. A unified species concept is a good descriptor of biodiversity D. Type I grey zone: the species concepts produce a series of nested groups. Ranking these groups is an issue. E. Type II grey zone: the species concepts produce partially non-nested groups. Inter- and intra-approach pluralism can be problematic. For cases D & E, pragmatic descriptors would be more accurate and informative about biodiversity than a unified species concept.

Mentions: There are good reasons for this choice: species pose at least two major problems to microbial diversity studies. First, species raise the problem of inter-approach pluralism[37]. Microbiologists studying prokaryotes do not adhere to a single (unified) species concept[37]. Rather, they recognize different but equally legitimate rules (or 'species concepts') to group individual microbes as members of a given species taxon[37]. These rules rest on distinct criteria, many of which are based on different evolutionary and ecological processes, capturing diverse important features of microbial diversity[38,39]. Consequently, there is no guarantee that individual microbes should always fall into recognizable discrete groups, showing tight genotypic and phenotypic similarity as well as genetic connectivity[40-43]. For a given set of individuals in a given environment, this plurality of legitimate rules can and does produce a plurality of valid incompatible groups[44-48] (Figure 1A). However, if different species concepts are used to assess the diversity in different environments, estimates of the number and composition of species are not directly comparable.


Some considerations for analyzing biodiversity using integrative metagenomics and gene networks.

Bittner L, Halary S, Payri C, Cruaud C, de Reviers B, Lopez P, Bapteste E - Biol. Direct (2010)

Four remarkable situations when distinct species concepts are applied. Each species concept groups a set of organisms, as members of a species taxon, as illustrated by a colored circle (purple for the phylogenetic species, green for the recombining or biological species, blue for the morphological species, pink for the barcode-based species). The overlap between groups is indicated by red dashes. A. In prokaryotes, the groups defined by the various species concepts are largely not nested. A unified species concept would be a poor descriptor of biodiversity: inter-approach pluralism is an issue for species definition. So is intra-approach pluralism, as indicated by smaller circles corresponding to the incongruent groups proposed by different markers, for a given species concept. B. Exploratory use of DNA barcoding to define groups of specimens belonging to a same species. On a histogram of p-distances frequencies, the identification of a barcode gap provides a threshold over which two specimens cannot belong to the same species. The monophyly of specimens falling in a same group can also be assessed. C. The ideal case: all the species concepts identify the same sets of organisms. Intra- and inter-approach pluralisms are not a problem. A unified species concept is a good descriptor of biodiversity D. Type I grey zone: the species concepts produce a series of nested groups. Ranking these groups is an issue. E. Type II grey zone: the species concepts produce partially non-nested groups. Inter- and intra-approach pluralism can be problematic. For cases D & E, pragmatic descriptors would be more accurate and informative about biodiversity than a unified species concept.
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Figure 1: Four remarkable situations when distinct species concepts are applied. Each species concept groups a set of organisms, as members of a species taxon, as illustrated by a colored circle (purple for the phylogenetic species, green for the recombining or biological species, blue for the morphological species, pink for the barcode-based species). The overlap between groups is indicated by red dashes. A. In prokaryotes, the groups defined by the various species concepts are largely not nested. A unified species concept would be a poor descriptor of biodiversity: inter-approach pluralism is an issue for species definition. So is intra-approach pluralism, as indicated by smaller circles corresponding to the incongruent groups proposed by different markers, for a given species concept. B. Exploratory use of DNA barcoding to define groups of specimens belonging to a same species. On a histogram of p-distances frequencies, the identification of a barcode gap provides a threshold over which two specimens cannot belong to the same species. The monophyly of specimens falling in a same group can also be assessed. C. The ideal case: all the species concepts identify the same sets of organisms. Intra- and inter-approach pluralisms are not a problem. A unified species concept is a good descriptor of biodiversity D. Type I grey zone: the species concepts produce a series of nested groups. Ranking these groups is an issue. E. Type II grey zone: the species concepts produce partially non-nested groups. Inter- and intra-approach pluralism can be problematic. For cases D & E, pragmatic descriptors would be more accurate and informative about biodiversity than a unified species concept.
Mentions: There are good reasons for this choice: species pose at least two major problems to microbial diversity studies. First, species raise the problem of inter-approach pluralism[37]. Microbiologists studying prokaryotes do not adhere to a single (unified) species concept[37]. Rather, they recognize different but equally legitimate rules (or 'species concepts') to group individual microbes as members of a given species taxon[37]. These rules rest on distinct criteria, many of which are based on different evolutionary and ecological processes, capturing diverse important features of microbial diversity[38,39]. Consequently, there is no guarantee that individual microbes should always fall into recognizable discrete groups, showing tight genotypic and phenotypic similarity as well as genetic connectivity[40-43]. For a given set of individuals in a given environment, this plurality of legitimate rules can and does produce a plurality of valid incompatible groups[44-48] (Figure 1A). However, if different species concepts are used to assess the diversity in different environments, estimates of the number and composition of species are not directly comparable.

Bottom Line: We reached these conclusions through a comparison of the theoretical foundations of two molecular approaches seeking to assess biodiversity: metagenomics (mostly used on prokaryotes and protists) and DNA barcoding (mostly used on multicellular eukaryotes), and by pragmatic considerations of the issues caused by the 'species problem' in biodiversity studies.Evolutionary gene networks reduce the risk of producing biodiversity estimates with limited explanatory power, biased either by unequal rates of LGT, or difficult to interpret due to (practical) problems caused by type I and type II grey zones.Moreover, these networks would easily accommodate additional (meta)transcriptomic and (meta)proteomic data.

View Article: PubMed Central - HTML - PubMed

Affiliation: UMR CNRS 7138 Systématique, Adaptation, Evolution, Université Pierre et Marie Curie, Paris, France.

ABSTRACT

Background: Improving knowledge of biodiversity will benefit conservation biology, enhance bioremediation studies, and could lead to new medical treatments. However there is no standard approach to estimate and to compare the diversity of different environments, or to study its past, and possibly, future evolution.

Presentation of the hypothesis: We argue that there are two conditions for significant progress in the identification and quantification of biodiversity. First, integrative metagenomic studies - aiming at the simultaneous examination (or even better at the integration) of observations about the elements, functions and evolutionary processes captured by the massive sequencing of multiple markers - should be preferred over DNA barcoding projects and over metagenomic projects based on a single marker. Second, such metagenomic data should be studied with novel inclusive network-based approaches, designed to draw inferences both on the many units and on the many processes present in the environments.

Testing the hypothesis: We reached these conclusions through a comparison of the theoretical foundations of two molecular approaches seeking to assess biodiversity: metagenomics (mostly used on prokaryotes and protists) and DNA barcoding (mostly used on multicellular eukaryotes), and by pragmatic considerations of the issues caused by the 'species problem' in biodiversity studies.

Implications of the hypothesis: Evolutionary gene networks reduce the risk of producing biodiversity estimates with limited explanatory power, biased either by unequal rates of LGT, or difficult to interpret due to (practical) problems caused by type I and type II grey zones. Moreover, these networks would easily accommodate additional (meta)transcriptomic and (meta)proteomic data.

Show MeSH