The microbial community associated with Parascaris spp. infecting juvenile horses

Jennifer L. Cain; Jamie K. Norris; Nichol E. Ripley; Parul Suri; Constance A. Finnerty; Holli S. Gravatte; Martin K. Nielsen

doi:10.1186/s13071-022-05533-y

The microbial community associated with Parascaris spp. infecting juvenile horses

Jennifer L. Cain, Jamie K. Norris, Nichol E. Ripley, Parul Suri, Constance A. Finnerty, Holli S. Gravatte, Martin K. Nielsen

Veterinary Science

Research output: Contribution to journal › Article › peer-review

Abstract

Background: Parasitic nematodes, including large roundworms colloquially known as ascarids, affect the health and well-being of livestock animals worldwide. The equine ascarids, Parascaris spp., are important parasites of juvenile horses and the first ascarids to develop widespread anthelmintic resistance. The microbiota has been shown to be an important factor in the fitness of many organisms, including parasitic nematodes, where endosymbiotic Wolbachia have been exploited for treatment of filariasis in humans. Methods: This study used short-read 16S rRNA sequences and Illumina sequencing to characterize and compare microbiota of whole worm small intestinal stages and microbiota of male and female intestines and gonads. Diversity metrics including alpha and beta diversity, and the differential abundance analyses DESeq2, ANCOM-BC, corncob, and metagenomeSeq were used for comparisons. Results: Alpha and beta diversity of whole worm microbiota did not differ significantly between groups, but Simpson alpha diversity was significantly different between female intestine (FI) and male gonad (MG) (P= 0.0018), and Shannon alpha diversity was significantly different between female and male gonads (P = 0.0130), FI and horse jejunum (HJ) (P = 0.0383), and FI and MG (P= 0.0001). Beta diversity (Fig. 2B) was significantly different between female and male gonads (P = 0.0006), male intestine (MI) and FG (P = 0.0093), and MG and FI (P = 0.0041). When comparing organs, Veillonella was differentially abundant for DESeq2 and ANCOM-BC (p < 0.0001), corncob (P = 0.0008), and metagenomeSeq (P = 0.0118), and Sarcina was differentially abundant across four methods (P < 0.0001). Finally, the microbiota of all individual Parascaris spp. specimens were compared to establish shared microbiota between groups. Conclusions: Overall, this study provided important information regarding the Parascaris spp. microbiota and provides a first step towards determining whether the microbiota may be a viable target for future parasite control options. Graphical abstract: [Figure not available: see fulltext.]

Original language	English
Article number	408
Journal	Parasites and Vectors
Volume	15
Issue number	1
DOIs	https://doi.org/10.1186/s13071-022-05533-y
State	Published - Dec 2022

Bibliographical note

Funding Information:
This work was supported by grants from Zoetis, Inc. ( https://www.zoetis.com/ ), Parsippany-Troy Hills, New Jersey and the National Center for Veterinary Parasitology ( https://www.ncvetp.org/ ), Stillwater, Oklahoma, both obtained by J.L.C. and M.K.N. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Funding Information:
The authors would like to thank the faculty and staff at the University of Kentucky Veterinary Diagnostic Laboratory, staff at the University of Kentucky Genomics Core Laboratory, and farm crew at the Main Chance Research Farm for all of their technical support. Jennifer Cain would also like to thank Christopher Cain for all of his help and support.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Ascarid
Equine parasite
Nematode
Parascaris
Parasite
Parasite microbiota

ASJC Scopus subject areas

Parasitology
Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1186/s13071-022-05533-y

Cite this

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title = "The microbial community associated with Parascaris spp. infecting juvenile horses",

abstract = "Background: Parasitic nematodes, including large roundworms colloquially known as ascarids, affect the health and well-being of livestock animals worldwide. The equine ascarids, Parascaris spp., are important parasites of juvenile horses and the first ascarids to develop widespread anthelmintic resistance. The microbiota has been shown to be an important factor in the fitness of many organisms, including parasitic nematodes, where endosymbiotic Wolbachia have been exploited for treatment of filariasis in humans. Methods: This study used short-read 16S rRNA sequences and Illumina sequencing to characterize and compare microbiota of whole worm small intestinal stages and microbiota of male and female intestines and gonads. Diversity metrics including alpha and beta diversity, and the differential abundance analyses DESeq2, ANCOM-BC, corncob, and metagenomeSeq were used for comparisons. Results: Alpha and beta diversity of whole worm microbiota did not differ significantly between groups, but Simpson alpha diversity was significantly different between female intestine (FI) and male gonad (MG) (P= 0.0018), and Shannon alpha diversity was significantly different between female and male gonads (P = 0.0130), FI and horse jejunum (HJ) (P = 0.0383), and FI and MG (P= 0.0001). Beta diversity (Fig. 2B) was significantly different between female and male gonads (P = 0.0006), male intestine (MI) and FG (P = 0.0093), and MG and FI (P = 0.0041). When comparing organs, Veillonella was differentially abundant for DESeq2 and ANCOM-BC (p < 0.0001), corncob (P = 0.0008), and metagenomeSeq (P = 0.0118), and Sarcina was differentially abundant across four methods (P < 0.0001). Finally, the microbiota of all individual Parascaris spp. specimens were compared to establish shared microbiota between groups. Conclusions: Overall, this study provided important information regarding the Parascaris spp. microbiota and provides a first step towards determining whether the microbiota may be a viable target for future parasite control options. Graphical abstract: [Figure not available: see fulltext.]",

keywords = "Ascarid, Equine parasite, Nematode, Parascaris, Parasite, Parasite microbiota",

author = "Cain, {Jennifer L.} and Norris, {Jamie K.} and Ripley, {Nichol E.} and Parul Suri and Finnerty, {Constance A.} and Gravatte, {Holli S.} and Nielsen, {Martin K.}",

note = "Funding Information: This work was supported by grants from Zoetis, Inc. ( https://www.zoetis.com/ ), Parsippany-Troy Hills, New Jersey and the National Center for Veterinary Parasitology ( https://www.ncvetp.org/ ), Stillwater, Oklahoma, both obtained by J.L.C. and M.K.N. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Funding Information: The authors would like to thank the faculty and staff at the University of Kentucky Veterinary Diagnostic Laboratory, staff at the University of Kentucky Genomics Core Laboratory, and farm crew at the Main Chance Research Farm for all of their technical support. Jennifer Cain would also like to thank Christopher Cain for all of his help and support. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s13071-022-05533-y",

language = "English",

volume = "15",

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TY - JOUR

T1 - The microbial community associated with Parascaris spp. infecting juvenile horses

AU - Cain, Jennifer L.

AU - Norris, Jamie K.

AU - Ripley, Nichol E.

AU - Suri, Parul

AU - Finnerty, Constance A.

AU - Gravatte, Holli S.

AU - Nielsen, Martin K.

N1 - Funding Information: This work was supported by grants from Zoetis, Inc. ( https://www.zoetis.com/ ), Parsippany-Troy Hills, New Jersey and the National Center for Veterinary Parasitology ( https://www.ncvetp.org/ ), Stillwater, Oklahoma, both obtained by J.L.C. and M.K.N. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Funding Information: The authors would like to thank the faculty and staff at the University of Kentucky Veterinary Diagnostic Laboratory, staff at the University of Kentucky Genomics Core Laboratory, and farm crew at the Main Chance Research Farm for all of their technical support. Jennifer Cain would also like to thank Christopher Cain for all of his help and support. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Parasitic nematodes, including large roundworms colloquially known as ascarids, affect the health and well-being of livestock animals worldwide. The equine ascarids, Parascaris spp., are important parasites of juvenile horses and the first ascarids to develop widespread anthelmintic resistance. The microbiota has been shown to be an important factor in the fitness of many organisms, including parasitic nematodes, where endosymbiotic Wolbachia have been exploited for treatment of filariasis in humans. Methods: This study used short-read 16S rRNA sequences and Illumina sequencing to characterize and compare microbiota of whole worm small intestinal stages and microbiota of male and female intestines and gonads. Diversity metrics including alpha and beta diversity, and the differential abundance analyses DESeq2, ANCOM-BC, corncob, and metagenomeSeq were used for comparisons. Results: Alpha and beta diversity of whole worm microbiota did not differ significantly between groups, but Simpson alpha diversity was significantly different between female intestine (FI) and male gonad (MG) (P= 0.0018), and Shannon alpha diversity was significantly different between female and male gonads (P = 0.0130), FI and horse jejunum (HJ) (P = 0.0383), and FI and MG (P= 0.0001). Beta diversity (Fig. 2B) was significantly different between female and male gonads (P = 0.0006), male intestine (MI) and FG (P = 0.0093), and MG and FI (P = 0.0041). When comparing organs, Veillonella was differentially abundant for DESeq2 and ANCOM-BC (p < 0.0001), corncob (P = 0.0008), and metagenomeSeq (P = 0.0118), and Sarcina was differentially abundant across four methods (P < 0.0001). Finally, the microbiota of all individual Parascaris spp. specimens were compared to establish shared microbiota between groups. Conclusions: Overall, this study provided important information regarding the Parascaris spp. microbiota and provides a first step towards determining whether the microbiota may be a viable target for future parasite control options. Graphical abstract: [Figure not available: see fulltext.]

AB - Background: Parasitic nematodes, including large roundworms colloquially known as ascarids, affect the health and well-being of livestock animals worldwide. The equine ascarids, Parascaris spp., are important parasites of juvenile horses and the first ascarids to develop widespread anthelmintic resistance. The microbiota has been shown to be an important factor in the fitness of many organisms, including parasitic nematodes, where endosymbiotic Wolbachia have been exploited for treatment of filariasis in humans. Methods: This study used short-read 16S rRNA sequences and Illumina sequencing to characterize and compare microbiota of whole worm small intestinal stages and microbiota of male and female intestines and gonads. Diversity metrics including alpha and beta diversity, and the differential abundance analyses DESeq2, ANCOM-BC, corncob, and metagenomeSeq were used for comparisons. Results: Alpha and beta diversity of whole worm microbiota did not differ significantly between groups, but Simpson alpha diversity was significantly different between female intestine (FI) and male gonad (MG) (P= 0.0018), and Shannon alpha diversity was significantly different between female and male gonads (P = 0.0130), FI and horse jejunum (HJ) (P = 0.0383), and FI and MG (P= 0.0001). Beta diversity (Fig. 2B) was significantly different between female and male gonads (P = 0.0006), male intestine (MI) and FG (P = 0.0093), and MG and FI (P = 0.0041). When comparing organs, Veillonella was differentially abundant for DESeq2 and ANCOM-BC (p < 0.0001), corncob (P = 0.0008), and metagenomeSeq (P = 0.0118), and Sarcina was differentially abundant across four methods (P < 0.0001). Finally, the microbiota of all individual Parascaris spp. specimens were compared to establish shared microbiota between groups. Conclusions: Overall, this study provided important information regarding the Parascaris spp. microbiota and provides a first step towards determining whether the microbiota may be a viable target for future parasite control options. Graphical abstract: [Figure not available: see fulltext.]

KW - Ascarid

KW - Equine parasite

KW - Nematode

KW - Parascaris

KW - Parasite

KW - Parasite microbiota

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U2 - 10.1186/s13071-022-05533-y

DO - 10.1186/s13071-022-05533-y

M3 - Article

C2 - 36333754

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VL - 15

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ER -

The microbial community associated with Parascaris spp. infecting juvenile horses

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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Cite this