The inadequacy of morphology for species and genus delineation in microbial eukaryotes: An example from the parabasalian termite symbiont Coronympha

James T. Harper, Gillian Gile, Erick R. James, Kevin J. Carpenter, Patrick J. Keeling

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Background: For the majority of microbial eukaryotes (protists, algae), there is no clearly superior species concept that is consistently applied. In the absence of a practical biological species concept, most species and genus level delineations have historically been based on morphology, which may lead to an underestimate of the diversity of microbial eukaryotes. Indeed, a growing body of molecular evidence, such as barcoding surveys, is beginning to support the conclusion that significant cryptic species diversity exists. This underestimate of diversity appears to be due to a combination of using morphology as the sole basis for assessing diversity and our inability to culture the vast majority of microbial life. Here we have used molecular markers to assess the species delineations in two related but morphologically distinct genera of uncultivated symbionts found in the hindgut of termites. Methodology/Principal Findings: Using single-cell isolation and environmental PCR, we have used a barcoding approach to characterize the diversity of Coronympha and Metacoronympha symbionts in four species of Incisitermes termites, which were also examined using scanning electron microscopy and light microcopy. Despite the fact that these genera are significantly different in morphological complexity and structural organisation, we find they are two life history stages of the same species. At the same time, we show that the symbionts from different termite hosts show an equal or greater level of sequence diversity than do the hosts, despite the fact that the symbionts are all classified as one species. Conclusions/Significance: The morphological information used to describe the diversity of these microbial symbionts is misleading at both the genus and species levels, and led to an underestimate of species level diversity as well as an overestimate of genus level diversity. The genus 'Metacoronympha' is invalid and appears to be a life history stage of Coronympha, while the single recognized species of Coronympha octonaria inhabiting these four termites is better described as four distinct species.

Original languageEnglish (US)
Article numbere6577
JournalPLoS One
Volume4
Issue number8
DOIs
StatePublished - Aug 11 2009
Externally publishedYes

Fingerprint

Isoptera
Eukaryota
symbionts
eukaryotic cells
Biodiversity
Algae
Life Cycle Stages
barcoding
algae
Incisitermes
Scanning electron microscopy
life history
Cell Separation
Electron Scanning Microscopy
hindgut
Light
scanning electron microscopy
Polymerase Chain Reaction
species diversity
genetic markers

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

The inadequacy of morphology for species and genus delineation in microbial eukaryotes : An example from the parabasalian termite symbiont Coronympha. / Harper, James T.; Gile, Gillian; James, Erick R.; Carpenter, Kevin J.; Keeling, Patrick J.

In: PLoS One, Vol. 4, No. 8, e6577, 11.08.2009.

Research output: Contribution to journalArticle

@article{e2b871a7d80949b6b97236d20dacfbfd,
title = "The inadequacy of morphology for species and genus delineation in microbial eukaryotes: An example from the parabasalian termite symbiont Coronympha",
abstract = "Background: For the majority of microbial eukaryotes (protists, algae), there is no clearly superior species concept that is consistently applied. In the absence of a practical biological species concept, most species and genus level delineations have historically been based on morphology, which may lead to an underestimate of the diversity of microbial eukaryotes. Indeed, a growing body of molecular evidence, such as barcoding surveys, is beginning to support the conclusion that significant cryptic species diversity exists. This underestimate of diversity appears to be due to a combination of using morphology as the sole basis for assessing diversity and our inability to culture the vast majority of microbial life. Here we have used molecular markers to assess the species delineations in two related but morphologically distinct genera of uncultivated symbionts found in the hindgut of termites. Methodology/Principal Findings: Using single-cell isolation and environmental PCR, we have used a barcoding approach to characterize the diversity of Coronympha and Metacoronympha symbionts in four species of Incisitermes termites, which were also examined using scanning electron microscopy and light microcopy. Despite the fact that these genera are significantly different in morphological complexity and structural organisation, we find they are two life history stages of the same species. At the same time, we show that the symbionts from different termite hosts show an equal or greater level of sequence diversity than do the hosts, despite the fact that the symbionts are all classified as one species. Conclusions/Significance: The morphological information used to describe the diversity of these microbial symbionts is misleading at both the genus and species levels, and led to an underestimate of species level diversity as well as an overestimate of genus level diversity. The genus 'Metacoronympha' is invalid and appears to be a life history stage of Coronympha, while the single recognized species of Coronympha octonaria inhabiting these four termites is better described as four distinct species.",
author = "Harper, {James T.} and Gillian Gile and James, {Erick R.} and Carpenter, {Kevin J.} and Keeling, {Patrick J.}",
year = "2009",
month = "8",
day = "11",
doi = "10.1371/journal.pone.0006577",
language = "English (US)",
volume = "4",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "8",

}

TY - JOUR

T1 - The inadequacy of morphology for species and genus delineation in microbial eukaryotes

T2 - An example from the parabasalian termite symbiont Coronympha

AU - Harper, James T.

AU - Gile, Gillian

AU - James, Erick R.

AU - Carpenter, Kevin J.

AU - Keeling, Patrick J.

PY - 2009/8/11

Y1 - 2009/8/11

N2 - Background: For the majority of microbial eukaryotes (protists, algae), there is no clearly superior species concept that is consistently applied. In the absence of a practical biological species concept, most species and genus level delineations have historically been based on morphology, which may lead to an underestimate of the diversity of microbial eukaryotes. Indeed, a growing body of molecular evidence, such as barcoding surveys, is beginning to support the conclusion that significant cryptic species diversity exists. This underestimate of diversity appears to be due to a combination of using morphology as the sole basis for assessing diversity and our inability to culture the vast majority of microbial life. Here we have used molecular markers to assess the species delineations in two related but morphologically distinct genera of uncultivated symbionts found in the hindgut of termites. Methodology/Principal Findings: Using single-cell isolation and environmental PCR, we have used a barcoding approach to characterize the diversity of Coronympha and Metacoronympha symbionts in four species of Incisitermes termites, which were also examined using scanning electron microscopy and light microcopy. Despite the fact that these genera are significantly different in morphological complexity and structural organisation, we find they are two life history stages of the same species. At the same time, we show that the symbionts from different termite hosts show an equal or greater level of sequence diversity than do the hosts, despite the fact that the symbionts are all classified as one species. Conclusions/Significance: The morphological information used to describe the diversity of these microbial symbionts is misleading at both the genus and species levels, and led to an underestimate of species level diversity as well as an overestimate of genus level diversity. The genus 'Metacoronympha' is invalid and appears to be a life history stage of Coronympha, while the single recognized species of Coronympha octonaria inhabiting these four termites is better described as four distinct species.

AB - Background: For the majority of microbial eukaryotes (protists, algae), there is no clearly superior species concept that is consistently applied. In the absence of a practical biological species concept, most species and genus level delineations have historically been based on morphology, which may lead to an underestimate of the diversity of microbial eukaryotes. Indeed, a growing body of molecular evidence, such as barcoding surveys, is beginning to support the conclusion that significant cryptic species diversity exists. This underestimate of diversity appears to be due to a combination of using morphology as the sole basis for assessing diversity and our inability to culture the vast majority of microbial life. Here we have used molecular markers to assess the species delineations in two related but morphologically distinct genera of uncultivated symbionts found in the hindgut of termites. Methodology/Principal Findings: Using single-cell isolation and environmental PCR, we have used a barcoding approach to characterize the diversity of Coronympha and Metacoronympha symbionts in four species of Incisitermes termites, which were also examined using scanning electron microscopy and light microcopy. Despite the fact that these genera are significantly different in morphological complexity and structural organisation, we find they are two life history stages of the same species. At the same time, we show that the symbionts from different termite hosts show an equal or greater level of sequence diversity than do the hosts, despite the fact that the symbionts are all classified as one species. Conclusions/Significance: The morphological information used to describe the diversity of these microbial symbionts is misleading at both the genus and species levels, and led to an underestimate of species level diversity as well as an overestimate of genus level diversity. The genus 'Metacoronympha' is invalid and appears to be a life history stage of Coronympha, while the single recognized species of Coronympha octonaria inhabiting these four termites is better described as four distinct species.

UR - http://www.scopus.com/inward/record.url?scp=68949126781&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=68949126781&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0006577

DO - 10.1371/journal.pone.0006577

M3 - Article

C2 - 19668363

AN - SCOPUS:68949126781

VL - 4

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 8

M1 - e6577

ER -