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Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure

BACKGROUND: Gut microbiome community composition differs between cervical cancer (CC) patients and healthy controls, and increased gut diversity is associated with improved outcomes after treatment. We proposed that functions of specific microbial species adjoining the mucus layer may directly impac...

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Autores principales: Karpinets, Tatiana V., Wu, Xiaogang, Solley, Travis, El Alam, Molly B., Sims, Travis T., Yoshida-Court, Kyoko, Lynn, Erica, Ahmed-Kaddar, Mustapha, Biegert, Greyson, Yue, Jingyan, Song, Xingzhi, Sun, Huandong, Petrosino, Joseph F., Mezzari, Melissa P., Okhuysen, Pablo, Eifel, Patricia J., Jhingran, Anuja, Lin, Lilie L., Schmeler, Kathleen M., Ramondetta, Lois, Ajami, Nadim, Jenq, Robert R., Futreal, Andrew, Zhang, Jianhua, Klopp, Ann H., Colbert, Lauren E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9438314/
https://www.ncbi.nlm.nih.gov/pubmed/36050658
http://dx.doi.org/10.1186/s12885-022-09997-0
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author Karpinets, Tatiana V.
Wu, Xiaogang
Solley, Travis
El Alam, Molly B.
Sims, Travis T.
Yoshida-Court, Kyoko
Lynn, Erica
Ahmed-Kaddar, Mustapha
Biegert, Greyson
Yue, Jingyan
Song, Xingzhi
Sun, Huandong
Petrosino, Joseph F.
Mezzari, Melissa P.
Okhuysen, Pablo
Eifel, Patricia J.
Jhingran, Anuja
Lin, Lilie L.
Schmeler, Kathleen M.
Ramondetta, Lois
Ajami, Nadim
Jenq, Robert R.
Futreal, Andrew
Zhang, Jianhua
Klopp, Ann H.
Colbert, Lauren E.
author_facet Karpinets, Tatiana V.
Wu, Xiaogang
Solley, Travis
El Alam, Molly B.
Sims, Travis T.
Yoshida-Court, Kyoko
Lynn, Erica
Ahmed-Kaddar, Mustapha
Biegert, Greyson
Yue, Jingyan
Song, Xingzhi
Sun, Huandong
Petrosino, Joseph F.
Mezzari, Melissa P.
Okhuysen, Pablo
Eifel, Patricia J.
Jhingran, Anuja
Lin, Lilie L.
Schmeler, Kathleen M.
Ramondetta, Lois
Ajami, Nadim
Jenq, Robert R.
Futreal, Andrew
Zhang, Jianhua
Klopp, Ann H.
Colbert, Lauren E.
author_sort Karpinets, Tatiana V.
collection PubMed
description BACKGROUND: Gut microbiome community composition differs between cervical cancer (CC) patients and healthy controls, and increased gut diversity is associated with improved outcomes after treatment. We proposed that functions of specific microbial species adjoining the mucus layer may directly impact the biology of CC. METHOD: Metagenomes of rectal swabs in 41 CC patients were examined by whole-genome shotgun sequencing to link taxonomic structures, molecular functions, and metabolic pathway to patient’s clinical characteristics. RESULTS: Significant association of molecular functions encoded by the metagenomes was found with initial tumor size and stage. Profiling of the molecular function abundances and their distributions identified 2 microbial communities co-existing in each metagenome but having distinct metabolism and taxonomic structures. Community A (Clostridia and Proteobacteria predominant) was characterized by high activity of pathways involved in stress response, mucus glycan degradation and utilization of degradation byproducts. This community was prevalent in patients with larger, advanced stage tumors. Conversely, community B (Bacteroidia predominant) was characterized by fast growth, active oxidative phosphorylation, and production of vitamins. This community was prevalent in patients with smaller, early-stage tumors. CONCLUSIONS: In this study, enrichment of mucus degrading microbial communities in rectal metagenomes of CC patients was associated with larger, more advanced stage tumors. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12885-022-09997-0.
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spelling pubmed-94383142022-09-03 Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure Karpinets, Tatiana V. Wu, Xiaogang Solley, Travis El Alam, Molly B. Sims, Travis T. Yoshida-Court, Kyoko Lynn, Erica Ahmed-Kaddar, Mustapha Biegert, Greyson Yue, Jingyan Song, Xingzhi Sun, Huandong Petrosino, Joseph F. Mezzari, Melissa P. Okhuysen, Pablo Eifel, Patricia J. Jhingran, Anuja Lin, Lilie L. Schmeler, Kathleen M. Ramondetta, Lois Ajami, Nadim Jenq, Robert R. Futreal, Andrew Zhang, Jianhua Klopp, Ann H. Colbert, Lauren E. BMC Cancer Research Article BACKGROUND: Gut microbiome community composition differs between cervical cancer (CC) patients and healthy controls, and increased gut diversity is associated with improved outcomes after treatment. We proposed that functions of specific microbial species adjoining the mucus layer may directly impact the biology of CC. METHOD: Metagenomes of rectal swabs in 41 CC patients were examined by whole-genome shotgun sequencing to link taxonomic structures, molecular functions, and metabolic pathway to patient’s clinical characteristics. RESULTS: Significant association of molecular functions encoded by the metagenomes was found with initial tumor size and stage. Profiling of the molecular function abundances and their distributions identified 2 microbial communities co-existing in each metagenome but having distinct metabolism and taxonomic structures. Community A (Clostridia and Proteobacteria predominant) was characterized by high activity of pathways involved in stress response, mucus glycan degradation and utilization of degradation byproducts. This community was prevalent in patients with larger, advanced stage tumors. Conversely, community B (Bacteroidia predominant) was characterized by fast growth, active oxidative phosphorylation, and production of vitamins. This community was prevalent in patients with smaller, early-stage tumors. CONCLUSIONS: In this study, enrichment of mucus degrading microbial communities in rectal metagenomes of CC patients was associated with larger, more advanced stage tumors. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12885-022-09997-0. BioMed Central 2022-09-01 /pmc/articles/PMC9438314/ /pubmed/36050658 http://dx.doi.org/10.1186/s12885-022-09997-0 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 Article
Karpinets, Tatiana V.
Wu, Xiaogang
Solley, Travis
El Alam, Molly B.
Sims, Travis T.
Yoshida-Court, Kyoko
Lynn, Erica
Ahmed-Kaddar, Mustapha
Biegert, Greyson
Yue, Jingyan
Song, Xingzhi
Sun, Huandong
Petrosino, Joseph F.
Mezzari, Melissa P.
Okhuysen, Pablo
Eifel, Patricia J.
Jhingran, Anuja
Lin, Lilie L.
Schmeler, Kathleen M.
Ramondetta, Lois
Ajami, Nadim
Jenq, Robert R.
Futreal, Andrew
Zhang, Jianhua
Klopp, Ann H.
Colbert, Lauren E.
Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title_full Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title_fullStr Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title_full_unstemmed Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title_short Metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
title_sort metagenomes of rectal swabs in larger, advanced stage cervical cancers have enhanced mucus degrading functionalities and distinct taxonomic structure
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9438314/
https://www.ncbi.nlm.nih.gov/pubmed/36050658
http://dx.doi.org/10.1186/s12885-022-09997-0
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