Cargando…

Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster

BACKGROUND: Visceral leishmaniasis (VL) is the most severe form of all leishmanial infections and is caused by infection with protozoa of Leishmania donovani and Leishmania infantum. This parasitic disease occurs in over 80 countries and its geographic distribution is on the rise. Although the inter...

Descripción completa

Detalles Bibliográficos
Autores principales: Olías-Molero, Ana Isabel, Botías, Pedro, Cuquerella, Montserrat, García-Cantalejo, Jesús, Barcia, Emilia, Torrado, Susana, Torrado, Juan José, Alunda, José María
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9753363/
https://www.ncbi.nlm.nih.gov/pubmed/36522762
http://dx.doi.org/10.1186/s13071-022-05576-1
_version_ 1784850947700162560
author Olías-Molero, Ana Isabel
Botías, Pedro
Cuquerella, Montserrat
García-Cantalejo, Jesús
Barcia, Emilia
Torrado, Susana
Torrado, Juan José
Alunda, José María
author_facet Olías-Molero, Ana Isabel
Botías, Pedro
Cuquerella, Montserrat
García-Cantalejo, Jesús
Barcia, Emilia
Torrado, Susana
Torrado, Juan José
Alunda, José María
author_sort Olías-Molero, Ana Isabel
collection PubMed
description BACKGROUND: Visceral leishmaniasis (VL) is the most severe form of all leishmanial infections and is caused by infection with protozoa of Leishmania donovani and Leishmania infantum. This parasitic disease occurs in over 80 countries and its geographic distribution is on the rise. Although the interaction between the intestinal microbiome and the immune response has been established in several pathologies, it has not been widely studied in leishmaniasis. The Syrian hamster is the most advanced laboratory model for developing vaccines and new drugs against VL. In the study reported here, we explored the relationship between the intestinal microbiome and infection with L. infantum in this surrogate host. METHODS: Male Syrian hamsters (120–140 g) were inoculated with 10(8) promastigotes of a canine-derived L. infantum strain or left as uninfected control animals. Infection was maintained for 19 weeks (endpoint) and monitored by an immunoglobulin G (IgG) enyzme-linked immunosorbent assay throughout the experiment. Individual faecal samples, obtained at weeks 16, 18 and 19 post-inoculation, were analysed to determine the 16S metagenomic composition (the operational taxonomic units [OTUs] of the intestinal microbiome and the comparison between groups were FDR (false discovery rate)-adjusted). RESULTS: Leishmania infantum infection elicited moderate clinical signs and lesions and a steady increase in specific anti-Leishmania serum IgG. The predominant phyla (Firmicutes + Bacteriodetes: > 90%), families (Muribaculaceae + Lachnospiraceae + Ruminococcaceae: 70–80%) and genera found in the uninfected hamsters showed no significant variations throughout the experiment. Leishmania infantum infection provoked a slightly higher—albeit non-significant—value for the Firmicutes/Bacteriodetes ratio but no notable differences were found in the relative abundance or diversity of phyla and families. The microbiome of the infected hamsters was enriched in CAG-352, whereas Lachnospiraceae UCG-004, the [Eubacterium] ventriosum group and Allobaculum were less abundant. CONCLUSIONS: The lack of extensive significant differences between hamsters infected and uninfected with L. infantum in the higher taxa (phyla, families) and the scarce variation found, which was restricted to genera with a low relative abundance, suggest that there is no clear VL infection-intestinal microbiome axis in hamsters. Further studies are needed (chronic infections, co-abundance analyses, intestinal sampling, functional analysis) to confirm these findings and to determine more precisely the possible relationship between microbiome composition and VL infection. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05576-1.
format Online
Article
Text
id pubmed-9753363
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-97533632022-12-16 Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster Olías-Molero, Ana Isabel Botías, Pedro Cuquerella, Montserrat García-Cantalejo, Jesús Barcia, Emilia Torrado, Susana Torrado, Juan José Alunda, José María Parasit Vectors Research BACKGROUND: Visceral leishmaniasis (VL) is the most severe form of all leishmanial infections and is caused by infection with protozoa of Leishmania donovani and Leishmania infantum. This parasitic disease occurs in over 80 countries and its geographic distribution is on the rise. Although the interaction between the intestinal microbiome and the immune response has been established in several pathologies, it has not been widely studied in leishmaniasis. The Syrian hamster is the most advanced laboratory model for developing vaccines and new drugs against VL. In the study reported here, we explored the relationship between the intestinal microbiome and infection with L. infantum in this surrogate host. METHODS: Male Syrian hamsters (120–140 g) were inoculated with 10(8) promastigotes of a canine-derived L. infantum strain or left as uninfected control animals. Infection was maintained for 19 weeks (endpoint) and monitored by an immunoglobulin G (IgG) enyzme-linked immunosorbent assay throughout the experiment. Individual faecal samples, obtained at weeks 16, 18 and 19 post-inoculation, were analysed to determine the 16S metagenomic composition (the operational taxonomic units [OTUs] of the intestinal microbiome and the comparison between groups were FDR (false discovery rate)-adjusted). RESULTS: Leishmania infantum infection elicited moderate clinical signs and lesions and a steady increase in specific anti-Leishmania serum IgG. The predominant phyla (Firmicutes + Bacteriodetes: > 90%), families (Muribaculaceae + Lachnospiraceae + Ruminococcaceae: 70–80%) and genera found in the uninfected hamsters showed no significant variations throughout the experiment. Leishmania infantum infection provoked a slightly higher—albeit non-significant—value for the Firmicutes/Bacteriodetes ratio but no notable differences were found in the relative abundance or diversity of phyla and families. The microbiome of the infected hamsters was enriched in CAG-352, whereas Lachnospiraceae UCG-004, the [Eubacterium] ventriosum group and Allobaculum were less abundant. CONCLUSIONS: The lack of extensive significant differences between hamsters infected and uninfected with L. infantum in the higher taxa (phyla, families) and the scarce variation found, which was restricted to genera with a low relative abundance, suggest that there is no clear VL infection-intestinal microbiome axis in hamsters. Further studies are needed (chronic infections, co-abundance analyses, intestinal sampling, functional analysis) to confirm these findings and to determine more precisely the possible relationship between microbiome composition and VL infection. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05576-1. BioMed Central 2022-12-15 /pmc/articles/PMC9753363/ /pubmed/36522762 http://dx.doi.org/10.1186/s13071-022-05576-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Olías-Molero, Ana Isabel
Botías, Pedro
Cuquerella, Montserrat
García-Cantalejo, Jesús
Barcia, Emilia
Torrado, Susana
Torrado, Juan José
Alunda, José María
Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title_full Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title_fullStr Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title_full_unstemmed Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title_short Leishmania infantum infection does not affect the main composition of the intestinal microbiome of the Syrian hamster
title_sort leishmania infantum infection does not affect the main composition of the intestinal microbiome of the syrian hamster
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9753363/
https://www.ncbi.nlm.nih.gov/pubmed/36522762
http://dx.doi.org/10.1186/s13071-022-05576-1
work_keys_str_mv AT oliasmoleroanaisabel leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT botiaspedro leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT cuquerellamontserrat leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT garciacantalejojesus leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT barciaemilia leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT torradosusana leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT torradojuanjose leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster
AT alundajosemaria leishmaniainfantuminfectiondoesnotaffectthemaincompositionoftheintestinalmicrobiomeofthesyrianhamster