Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries

Culture-independent metagenomic methodologies have enabled detection and identification of microorganisms in various biological systems and often revealed complex and unknown microbiomes. In many organisms, the microbiome outnumbers the host cells and greatly affects the host biology and fitness. Ti...

Full description

Bibliographic Details
Main Authors: Melina Garcia Guizzo, Saraswoti Neupane, Matej Kucera, Jan Perner, Helena Frantová, Itabajara da Silva Vaz, Pedro L. de Oliveira, Petr Kopacek, Ludek Zurek
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2020.00211/full
id doaj-b5961608f3664f34804fea805545f807
record_format Article
spelling doaj-b5961608f3664f34804fea805545f8072020-11-25T02:09:34ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882020-05-011010.3389/fcimb.2020.00211515648Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in OvariesMelina Garcia Guizzo0Melina Garcia Guizzo1Saraswoti Neupane2Matej Kucera3Matej Kucera4Jan Perner5Helena Frantová6Itabajara da Silva Vaz7Itabajara da Silva Vaz8Pedro L. de Oliveira9Petr Kopacek10Ludek Zurek11Ludek Zurek12Central European Institute of Technology (CEITEC), Center for Zoonoses, University of Veterinary and Pharmaceutical Sciences, Brno, CzechiaBiology Centre, Institute of Parasitology, Czech Academy of Sciences, Ceske Budejovice, CzechiaDepartment of Entomology, Kansas State University, Manhattan, KS, United StatesBiology Centre, Institute of Parasitology, Czech Academy of Sciences, Ceske Budejovice, CzechiaFaculty of Science, University of South Bohemia, Ceske Budejovice, CzechiaBiology Centre, Institute of Parasitology, Czech Academy of Sciences, Ceske Budejovice, CzechiaBiology Centre, Institute of Parasitology, Czech Academy of Sciences, Ceske Budejovice, CzechiaLaboratório de Imunologia Aplicada a Sanidade Animal, Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, BrazilFaculdade de Veterinária, Universidade Federal do Rio Grande do Sul, Porto Alegre, BrazilLaboratório de Bioquímica de Artrópodes Hematófagos, Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilBiology Centre, Institute of Parasitology, Czech Academy of Sciences, Ceske Budejovice, CzechiaCentral European Institute of Technology (CEITEC), Center for Zoonoses, University of Veterinary and Pharmaceutical Sciences, Brno, CzechiaDepartment of Chemistry and Biochemistry, Mendel University, Brno, CzechiaCulture-independent metagenomic methodologies have enabled detection and identification of microorganisms in various biological systems and often revealed complex and unknown microbiomes. In many organisms, the microbiome outnumbers the host cells and greatly affects the host biology and fitness. Ticks are hematophagous ectoparasites with a wide host range. They vector a number of human and animal pathogens and also directly cause major economic losses in livestock. Although several reports on a tick midgut microbiota show a diverse bacterial community, in most cases the size of the bacterial population has not been determined. In this study, the microbiome was quantified in the midgut and ovaries of the ticks Ixodes ricinus and Rhipicephalus microplus before, during, and after blood feeding. Although the size of bacterial community in the midgut fluctuated with blood feeding, it was overall extremely low in comparison to that of other hematophagous arthropods. In addition, the tick ovarian microbiome of both tick species exceeded the midgut 16S rDNA copy numbers by several orders of magnitude. This indicates that the ratio of a tick midgut/ovary microbiome represents an exception to the general biology of other metazoans. In addition to the very low abundance, the tick midgut diversity in I. ricinus was variable and that is in contrast to that found in the tick ovary. The ovary of I. ricinus had a very low bacterial diversity and a very high and stable bacterial abundance with the dominant endosymbiont, Midichloria sp. The elucidation of this aspect of tick biology highlights a unique tissue-specific microbial-invertebrate host interaction.https://www.frontiersin.org/article/10.3389/fcimb.2020.00211/fulltickIxodes ricinusRhipicephalus microplusmidgut microbiomeovary microbiomesymbiosis
collection DOAJ
language English
format Article
sources DOAJ
author Melina Garcia Guizzo
Melina Garcia Guizzo
Saraswoti Neupane
Matej Kucera
Matej Kucera
Jan Perner
Helena Frantová
Itabajara da Silva Vaz
Itabajara da Silva Vaz
Pedro L. de Oliveira
Petr Kopacek
Ludek Zurek
Ludek Zurek
spellingShingle Melina Garcia Guizzo
Melina Garcia Guizzo
Saraswoti Neupane
Matej Kucera
Matej Kucera
Jan Perner
Helena Frantová
Itabajara da Silva Vaz
Itabajara da Silva Vaz
Pedro L. de Oliveira
Petr Kopacek
Ludek Zurek
Ludek Zurek
Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
Frontiers in Cellular and Infection Microbiology
tick
Ixodes ricinus
Rhipicephalus microplus
midgut microbiome
ovary microbiome
symbiosis
author_facet Melina Garcia Guizzo
Melina Garcia Guizzo
Saraswoti Neupane
Matej Kucera
Matej Kucera
Jan Perner
Helena Frantová
Itabajara da Silva Vaz
Itabajara da Silva Vaz
Pedro L. de Oliveira
Petr Kopacek
Ludek Zurek
Ludek Zurek
author_sort Melina Garcia Guizzo
title Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
title_short Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
title_full Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
title_fullStr Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
title_full_unstemmed Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries
title_sort poor unstable midgut microbiome of hard ticks contrasts with abundant and stable monospecific microbiome in ovaries
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2020-05-01
description Culture-independent metagenomic methodologies have enabled detection and identification of microorganisms in various biological systems and often revealed complex and unknown microbiomes. In many organisms, the microbiome outnumbers the host cells and greatly affects the host biology and fitness. Ticks are hematophagous ectoparasites with a wide host range. They vector a number of human and animal pathogens and also directly cause major economic losses in livestock. Although several reports on a tick midgut microbiota show a diverse bacterial community, in most cases the size of the bacterial population has not been determined. In this study, the microbiome was quantified in the midgut and ovaries of the ticks Ixodes ricinus and Rhipicephalus microplus before, during, and after blood feeding. Although the size of bacterial community in the midgut fluctuated with blood feeding, it was overall extremely low in comparison to that of other hematophagous arthropods. In addition, the tick ovarian microbiome of both tick species exceeded the midgut 16S rDNA copy numbers by several orders of magnitude. This indicates that the ratio of a tick midgut/ovary microbiome represents an exception to the general biology of other metazoans. In addition to the very low abundance, the tick midgut diversity in I. ricinus was variable and that is in contrast to that found in the tick ovary. The ovary of I. ricinus had a very low bacterial diversity and a very high and stable bacterial abundance with the dominant endosymbiont, Midichloria sp. The elucidation of this aspect of tick biology highlights a unique tissue-specific microbial-invertebrate host interaction.
topic tick
Ixodes ricinus
Rhipicephalus microplus
midgut microbiome
ovary microbiome
symbiosis
url https://www.frontiersin.org/article/10.3389/fcimb.2020.00211/full
work_keys_str_mv AT melinagarciaguizzo poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT melinagarciaguizzo poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT saraswotineupane poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT matejkucera poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT matejkucera poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT janperner poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT helenafrantova poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT itabajaradasilvavaz poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT itabajaradasilvavaz poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT pedroldeoliveira poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT petrkopacek poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT ludekzurek poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
AT ludekzurek poorunstablemidgutmicrobiomeofhardtickscontrastswithabundantandstablemonospecificmicrobiomeinovaries
_version_ 1724922970765262848