Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
ABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infect...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-10-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01705-20 |
| _version_ | 1818844382925684736 |
|---|---|
| author | Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke |
| author_facet | Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke |
| author_sort | Alice V. Easton |
| collection | DOAJ |
| description | ABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infected with STH alone, or not infected with either P. vivax or STH. In addition to a complete blood count (CBC) with differential, transcriptional profiling of peripheral blood samples was performed by transcriptome sequencing (RNA-Seq), fecal microbial communities were determined by 16S rRNA gene sequencing, and circulating cytokine levels were measured by bead-based immunoassays. Differences in blood cell counts, including an increased percentage of neutrophils, associated with a transcriptional signature of neutrophil activation, were driven primarily by P. vivax infection. P. vivax infection was also associated with increased levels of interleukin 6 (IL-6), IL-8, and IL-10; these cytokine levels were not affected by STH coinfection. Surprisingly, P. vivax infection was more strongly associated with differences in the microbiota than STH infection. Children infected with only P. vivax exhibited elevated Bacteroides and reduced Prevotella and Clostridiaceae levels, but these differences were not observed in individuals coinfected with STH. We also observed that P. vivax parasitemia was higher in the STH-infected population. When we used machine learning to identify the most important predictors of the P. vivax parasite burden (among P. vivax-infected individuals), bacterial taxa were the strongest predictors of parasitemia. In contrast, circulating transforming growth factor β (TGF-β) was the strongest predictor of the Trichuris trichiura egg burden. This study provides unexpected evidence that the gut microbiota may have a stronger link with P. vivax than with STH infection. IMPORTANCE Plasmodium (malaria) and helminth parasite coinfections are frequent, and both infections can be affected by the host gut microbiota. However, the relationship between coinfection and the gut microbiota is unclear. By performing comprehensive analyses on blood/stool samples from 130 individuals in Colombia, we found that the gut microbiota may have a stronger relationship with the number of P. vivax (malaria) parasites than with the number of helminth parasites infecting a host. Microbiota analysis identified more predictors of the P. vivax parasite burden, whereas analysis of blood samples identified predictors of the helminth parasite burden. These results were unexpected, because we expected each parasite to be associated with greater differences in its biological niche (blood for P. vivax and the intestine for helminths). Instead, we find that bacterial taxa were the strongest predictors of P. vivax parasitemia levels, while circulating TGF-β levels were the strongest predictor of helminth parasite burdens. |
| first_indexed | 2024-12-19T05:12:53Z |
| format | Article |
| id | doaj.art-ea1ee9d4557e4aadbe57d74532554d83 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T05:12:53Z |
| publishDate | 2020-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-ea1ee9d4557e4aadbe57d74532554d832022-12-21T20:34:45ZengAmerican Society for MicrobiologymBio2150-75112020-10-0111510.1128/mBio.01705-20Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted HelminthsAlice V. Easton0Mayra Raciny-Aleman1Victor Liu2Erica Ruan3Christian Marier4Adriana Heguy5Maria Fernanda Yasnot6Ana Rodriguez7P’ng Loke8Department of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USAGenome Technology Center, Division of Advanced Research Technologies, New York University School of Medicine, New York, New York, USAGenome Technology Center, Division of Advanced Research Technologies, New York University School of Medicine, New York, New York, USACórdoba Microbiological and Biomedical Research Group, Universidad de Córdoba, Montería, ColombiaDepartment of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USAABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infected with STH alone, or not infected with either P. vivax or STH. In addition to a complete blood count (CBC) with differential, transcriptional profiling of peripheral blood samples was performed by transcriptome sequencing (RNA-Seq), fecal microbial communities were determined by 16S rRNA gene sequencing, and circulating cytokine levels were measured by bead-based immunoassays. Differences in blood cell counts, including an increased percentage of neutrophils, associated with a transcriptional signature of neutrophil activation, were driven primarily by P. vivax infection. P. vivax infection was also associated with increased levels of interleukin 6 (IL-6), IL-8, and IL-10; these cytokine levels were not affected by STH coinfection. Surprisingly, P. vivax infection was more strongly associated with differences in the microbiota than STH infection. Children infected with only P. vivax exhibited elevated Bacteroides and reduced Prevotella and Clostridiaceae levels, but these differences were not observed in individuals coinfected with STH. We also observed that P. vivax parasitemia was higher in the STH-infected population. When we used machine learning to identify the most important predictors of the P. vivax parasite burden (among P. vivax-infected individuals), bacterial taxa were the strongest predictors of parasitemia. In contrast, circulating transforming growth factor β (TGF-β) was the strongest predictor of the Trichuris trichiura egg burden. This study provides unexpected evidence that the gut microbiota may have a stronger link with P. vivax than with STH infection. IMPORTANCE Plasmodium (malaria) and helminth parasite coinfections are frequent, and both infections can be affected by the host gut microbiota. However, the relationship between coinfection and the gut microbiota is unclear. By performing comprehensive analyses on blood/stool samples from 130 individuals in Colombia, we found that the gut microbiota may have a stronger relationship with the number of P. vivax (malaria) parasites than with the number of helminth parasites infecting a host. Microbiota analysis identified more predictors of the P. vivax parasite burden, whereas analysis of blood samples identified predictors of the helminth parasite burden. These results were unexpected, because we expected each parasite to be associated with greater differences in its biological niche (blood for P. vivax and the intestine for helminths). Instead, we find that bacterial taxa were the strongest predictors of P. vivax parasitemia levels, while circulating TGF-β levels were the strongest predictor of helminth parasite burdens.https://journals.asm.org/doi/10.1128/mBio.01705-20ColombiaPlasmodium vivaxSTHsoil-transmitted helminthsTrichuris trichiuramalaria |
| spellingShingle | Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths mBio Colombia Plasmodium vivax STH soil-transmitted helminths Trichuris trichiura malaria |
| title | Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths |
| title_full | Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths |
| title_fullStr | Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths |
| title_full_unstemmed | Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths |
| title_short | Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths |
| title_sort | immune response and microbiota profiles during coinfection with named content content type genus species plasmodium vivax named content and soil transmitted helminths |
| topic | Colombia Plasmodium vivax STH soil-transmitted helminths Trichuris trichiura malaria |
| url | https://journals.asm.org/doi/10.1128/mBio.01705-20 |
| work_keys_str_mv | AT aliceveaston immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT mayraracinyaleman immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT victorliu immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT ericaruan immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT christianmarier immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT adrianaheguy immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT mariafernandayasnot immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT anarodriguez immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths AT pngloke immuneresponseandmicrobiotaprofilesduringcoinfectionwithnamedcontentcontenttypegenusspeciesplasmodiumvivaxnamedcontentandsoiltransmittedhelminths |