Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar

Research on the gut microbiome may help with increasing our understanding of primate health with species’ ecology, evolution, and behavior. In particular, microbiome-related information has the potential to clarify ecology issues, providing knowledge in support of wild primates conservation and thei...

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Main Authors: Federico Correa, Valeria Torti, Caterina Spiezio, Alice Checcucci, Monica Modesto, Luigimaria Borruso, Luciano Cavani, Tanja Mimmo, Stefano Cesco, Diana Luise, Rose M. Randrianarison, Marco Gamba, Nianja J. Rarojoson, Maurizio Sanguinetti, Maura Di Vito, Francesca Bugli, Paola Mattarelli, Paolo Trevisi, Cristina Giacoma, Camillo Sandri
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.668274/full
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author Federico Correa
Valeria Torti
Caterina Spiezio
Alice Checcucci
Monica Modesto
Luigimaria Borruso
Luciano Cavani
Tanja Mimmo
Stefano Cesco
Diana Luise
Rose M. Randrianarison
Rose M. Randrianarison
Marco Gamba
Nianja J. Rarojoson
Maurizio Sanguinetti
Maurizio Sanguinetti
Maura Di Vito
Francesca Bugli
Francesca Bugli
Paola Mattarelli
Paolo Trevisi
Cristina Giacoma
Camillo Sandri
Camillo Sandri
spellingShingle Federico Correa
Valeria Torti
Caterina Spiezio
Alice Checcucci
Monica Modesto
Luigimaria Borruso
Luciano Cavani
Tanja Mimmo
Stefano Cesco
Diana Luise
Rose M. Randrianarison
Rose M. Randrianarison
Marco Gamba
Nianja J. Rarojoson
Maurizio Sanguinetti
Maurizio Sanguinetti
Maura Di Vito
Francesca Bugli
Francesca Bugli
Paola Mattarelli
Paolo Trevisi
Cristina Giacoma
Camillo Sandri
Camillo Sandri
Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
Frontiers in Microbiology
gut microbiome
soil quality
non-human primate
animal ecology
endangered species
geophagy
author_facet Federico Correa
Valeria Torti
Caterina Spiezio
Alice Checcucci
Monica Modesto
Luigimaria Borruso
Luciano Cavani
Tanja Mimmo
Stefano Cesco
Diana Luise
Rose M. Randrianarison
Rose M. Randrianarison
Marco Gamba
Nianja J. Rarojoson
Maurizio Sanguinetti
Maurizio Sanguinetti
Maura Di Vito
Francesca Bugli
Francesca Bugli
Paola Mattarelli
Paolo Trevisi
Cristina Giacoma
Camillo Sandri
Camillo Sandri
author_sort Federico Correa
title Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
title_short Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
title_full Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
title_fullStr Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
title_full_unstemmed Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar
title_sort disentangling the possible drivers of indri indri microbiome: a threatened lemur species of madagascar
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-08-01
description Research on the gut microbiome may help with increasing our understanding of primate health with species’ ecology, evolution, and behavior. In particular, microbiome-related information has the potential to clarify ecology issues, providing knowledge in support of wild primates conservation and their associated habitats. Indri (Indri indri) is the largest extant living lemur of Madagascar. This species is classified as “critically endangered” by the IUCN Red List of Threatened Species, representing one of the world’s 25 most endangered primates. Indris diet is mainly folivorous, but these primates frequently and voluntarily engage in geophagy. Indris have never been successfully bred under human care, suggesting that some behavioral and/or ecological factors are still not considered from the ex situ conservation protocols. Here, we explored gut microbiome composition of 18 indris belonging to 5 different family groups. The most represented phyla were Proteobacteria 40.1 ± 9.5%, Bacteroidetes 28.7 ± 2.8%, Synergistetes 16.7 ± 4.5%, and Firmicutes 11.1 ± 1.9%. Further, our results revealed that bacterial alpha and beta diversity were influenced by indri family group and sex. In addition, we investigated the chemical composition of geophagic soil to explore the possible ecological value of soil as a nutrient supply. The quite acidic pH and high levels of secondary oxide-hydroxides of the soils could play a role in the folivorous diet’s gut detoxification activity. In addition, the high contents of iron and manganese found the soils could act as micronutrients in the indris’ diet. Nevertheless, the concentration of a few elements (i.e., calcium, sulfur, boron, nickel, sodium, and chromium) was higher in non-geophagic than in geophagic soils. In conclusion, the data presented herein provide a baseline for outlining some possible drivers responsible for the gut microbiome diversity in indris, thus laying the foundations for developing further strategies involved in indris’ conservation.
topic gut microbiome
soil quality
non-human primate
animal ecology
endangered species
geophagy
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.668274/full
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spelling doaj-910e6f0c6d3646f8869b416d6f8d6da02021-08-06T08:16:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-08-011210.3389/fmicb.2021.668274668274Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of MadagascarFederico Correa0Valeria Torti1Caterina Spiezio2Alice Checcucci3Monica Modesto4Luigimaria Borruso5Luciano Cavani6Tanja Mimmo7Stefano Cesco8Diana Luise9Rose M. Randrianarison10Rose M. Randrianarison11Marco Gamba12Nianja J. Rarojoson13Maurizio Sanguinetti14Maurizio Sanguinetti15Maura Di Vito16Francesca Bugli17Francesca Bugli18Paola Mattarelli19Paolo Trevisi20Cristina Giacoma21Camillo Sandri22Camillo Sandri23Department of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Life Sciences and Systems Biology, University of Torino, Turin, ItalyDepartment of Animal Health Care and Management, Parco Natura Viva – Garda Zoological Park, Verona, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyFaculty of Science and Technology, Free University of Bolzano-Bozen, Bolzano, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyFaculty of Science and Technology, Free University of Bolzano-Bozen, Bolzano, ItalyFaculty of Science and Technology, Free University of Bolzano-Bozen, Bolzano, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyGroupe d’Étude et de Recherche sur les Primates de Madagascar, Antananarivo, MadagascarMention d’Anthropobiologie et de Deìveloppement Durable, Université de Antananarivo, Antananarivo, MadagascarDepartment of Life Sciences and Systems Biology, University of Torino, Turin, ItalyLaboratoire de Pédologie, FOFIFA à Tsimbazaza, Antananarivo, MadagascarDipartimento di Scienze Biotecnologiche di Base, Cliniche Intensivologiche e Perioperatorie, Università Cattolica del Sacro Cuore, Rome, ItalyDipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, ItalyDipartimento di Scienze Biotecnologiche di Base, Cliniche Intensivologiche e Perioperatorie, Università Cattolica del Sacro Cuore, Rome, ItalyDipartimento di Scienze Biotecnologiche di Base, Cliniche Intensivologiche e Perioperatorie, Università Cattolica del Sacro Cuore, Rome, ItalyDipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Life Sciences and Systems Biology, University of Torino, Turin, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Animal Health Care and Management, Parco Natura Viva – Garda Zoological Park, Verona, ItalyResearch on the gut microbiome may help with increasing our understanding of primate health with species’ ecology, evolution, and behavior. In particular, microbiome-related information has the potential to clarify ecology issues, providing knowledge in support of wild primates conservation and their associated habitats. Indri (Indri indri) is the largest extant living lemur of Madagascar. This species is classified as “critically endangered” by the IUCN Red List of Threatened Species, representing one of the world’s 25 most endangered primates. Indris diet is mainly folivorous, but these primates frequently and voluntarily engage in geophagy. Indris have never been successfully bred under human care, suggesting that some behavioral and/or ecological factors are still not considered from the ex situ conservation protocols. Here, we explored gut microbiome composition of 18 indris belonging to 5 different family groups. The most represented phyla were Proteobacteria 40.1 ± 9.5%, Bacteroidetes 28.7 ± 2.8%, Synergistetes 16.7 ± 4.5%, and Firmicutes 11.1 ± 1.9%. Further, our results revealed that bacterial alpha and beta diversity were influenced by indri family group and sex. In addition, we investigated the chemical composition of geophagic soil to explore the possible ecological value of soil as a nutrient supply. The quite acidic pH and high levels of secondary oxide-hydroxides of the soils could play a role in the folivorous diet’s gut detoxification activity. In addition, the high contents of iron and manganese found the soils could act as micronutrients in the indris’ diet. Nevertheless, the concentration of a few elements (i.e., calcium, sulfur, boron, nickel, sodium, and chromium) was higher in non-geophagic than in geophagic soils. In conclusion, the data presented herein provide a baseline for outlining some possible drivers responsible for the gut microbiome diversity in indris, thus laying the foundations for developing further strategies involved in indris’ conservation.https://www.frontiersin.org/articles/10.3389/fmicb.2021.668274/fullgut microbiomesoil qualitynon-human primateanimal ecologyendangered speciesgeophagy