The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance

Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across diff...

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Published in:Frontiers in microbiology Vol. 7; no. 1472; p. 1472
Main Authors: Bouchon, Didier, Zimmer, Martin, Dittmer, Jessica
Format: Journal Article
Language:English
Published: Switzerland Frontiers Media 23.09.2016
Frontiers Media S.A
Subjects:
ecological interactions
Host-Symbiont Interactions
Life Sciences
Microbiology
microbiota
Symbiosis
Terrestrial isopods
bacterial diversity
microbiota
terrestrial isopods
ecological interactions
endosymbionts
symbiosis
ISSN:1664-302X, 1664-302X
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Abstract Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host-microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in the digestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Hepatoplasma crinochetorum, Hepatincola porcellionum, and ), while others are well-known intracellular pathogens ( spp.) or reproductive parasites ( sp.). Moreover, a recent investigation of the microbiota in has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbes in the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.
AbstractList Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host–microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in the digestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Candidatus Hepatoplasma crinochetorum, Candidatus Hepatincola porcellionum, and Rhabdochlamydia porcellionis), while others are well-known intracellular pathogens (Rickettsiella spp.) or reproductive parasites (Wolbachia sp.). Moreover, a recent investigation of the microbiota in Armadillidium vulgare has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbes in the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.
Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host-microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in the digestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Hepatoplasma crinochetorum, Hepatincola porcellionum, and ), while others are well-known intracellular pathogens ( spp.) or reproductive parasites ( sp.). Moreover, a recent investigation of the microbiota in has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbes in the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.
Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host–microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in thedigestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Candidatus Hepatoplasma crinochetorum, Candidatus Hepatincola porcellionum, and Rhabdochlamydia porcellionis), while others are wellknown intracellular pathogens (Rickettsiella spp.) or reproductive parasites (Wolbachia sp.). Moreover, a recent investigation of the microbiota in Armadillidium vulgare has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbesin the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.
Author Dittmer, Jessica
Zimmer, Martin
Bouchon, Didier
AuthorAffiliation 3 Rowland Institute at Harvard, Harvard University, Cambridge MA, USA
1 UMR CNRS 7267, Ecologie et Biologie des Interactions, Université de Poitiers Poitiers, France
2 Leibniz Center for Tropical Marine Ecology Bremen, Germany
AuthorAffiliation_xml – name: 2 Leibniz Center for Tropical Marine Ecology Bremen, Germany
– name: 1 UMR CNRS 7267, Ecologie et Biologie des Interactions, Université de Poitiers Poitiers, France
– name: 3 Rowland Institute at Harvard, Harvard University, Cambridge MA, USA
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ContentType Journal Article
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Issue 1472
Keywords bacterial diversity
microbiota
terrestrial isopods
ecological interactions
endosymbionts
symbiosis
Language English
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This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology
Reviewed by: Pepijn Wilhelmus Kooij, Royal Botanic Gardens, UK; Yuval Gottlieb, Hebrew University of Jerusalem, Israel; Yongjie Wang Wang, Shanghai Ocean University, China
Edited by: Ute Hentschel, GEOMAR – Helmholtz Centre for Ocean Research Kiel, Germany
ORCID 0000-0002-2600-9201
0000-0002-4938-408X
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crossref_primary_10_3389_fmicb_2016_01472
crossref_citationtrail_10_3389_fmicb_2016_01472
PublicationCentury 2000
PublicationDate 2016-09-23
PublicationDateYYYYMMDD 2016-09-23
PublicationDate_xml – month: 09
  year: 2016
  text: 2016-09-23
  day: 23
PublicationDecade 2010
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in microbiology
PublicationTitleAlternate Front Microbiol
PublicationYear 2016
Publisher Frontiers Media
Frontiers Media S.A
Publisher_xml – name: Frontiers Media
– name: Frontiers Media S.A
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Snippet Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and...
Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity and...
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SubjectTerms ecological interactions
Host-Symbiont Interactions
Life Sciences
Microbiology
microbiota
Symbiosis
Terrestrial isopods
Title The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance
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