Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota

TY - JOUR

T1 - Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota

AU - Newbold, Lindsay K.

AU - Burthe, Sarah J.

AU - Oliver, Anna E.

AU - Gweon, Hyun S.

AU - Barnes, Christopher James

AU - Daunt, Francis

AU - van der Gast, Christopher J.

PY - 2017/3/1

Y1 - 2017/3/1

N2 - Infection by gastrointestinal helminths of humans, livestock and wild animals is common, but the impact of such endoparasites on wild hosts and their gut microbiota represents an important overlooked component of population dynamics. Wild host gut microbiota and endoparasites occupy the same physical niche spaces with both affecting host nutrition and health. However, associations between the two are poorly understood. Here we used the commonly parasitized European shag (Phalacrocorax aristotelis) as a model wild host. Forty live adults from the same colony were sampled. Endoscopy was employed to quantify helminth infection in situ. Microbiota from the significantly distinct proventriculus (site of infection), cloacal and faecal gastrointestinal tract microbiomes were characterised using 16S rRNA gene-targeted high-throughput sequencing. We found increasingly strong associations between helminth infection and microbiota composition progressing away from the site of infection, observing a pronounced dysbiosis in microbiota when samples were partitioned into high- and low-burden groups. We posit this dysbiosis is predominately explained by helminths inducing an anti-inflammatory environment in the proventriculus, diverting host immune responses away from themselves. This study, within live wild animals, provides a vital foundation to better understand the mechanisms that underpin the three-way relationship between helminths, microbiota and hosts.

AB - Infection by gastrointestinal helminths of humans, livestock and wild animals is common, but the impact of such endoparasites on wild hosts and their gut microbiota represents an important overlooked component of population dynamics. Wild host gut microbiota and endoparasites occupy the same physical niche spaces with both affecting host nutrition and health. However, associations between the two are poorly understood. Here we used the commonly parasitized European shag (Phalacrocorax aristotelis) as a model wild host. Forty live adults from the same colony were sampled. Endoscopy was employed to quantify helminth infection in situ. Microbiota from the significantly distinct proventriculus (site of infection), cloacal and faecal gastrointestinal tract microbiomes were characterised using 16S rRNA gene-targeted high-throughput sequencing. We found increasingly strong associations between helminth infection and microbiota composition progressing away from the site of infection, observing a pronounced dysbiosis in microbiota when samples were partitioned into high- and low-burden groups. We posit this dysbiosis is predominately explained by helminths inducing an anti-inflammatory environment in the proventriculus, diverting host immune responses away from themselves. This study, within live wild animals, provides a vital foundation to better understand the mechanisms that underpin the three-way relationship between helminths, microbiota and hosts.

KW - Animals

KW - Ascaridida Infections/parasitology

KW - Ascaridoidea/classification

KW - Bird Diseases/parasitology

KW - Birds/classification

KW - Female

KW - Gastrointestinal Tract/parasitology

KW - Male

U2 - 10.1038/ismej.2016.153

DO - 10.1038/ismej.2016.153

M3 - Journal article

C2 - 27983724

SN - 1751-7362

VL - 11

SP - 663

EP - 675

JO - I S M E Journal

JF - I S M E Journal

IS - 3

ER -