PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities

ABSTRACT Phylogeny is a powerful tool that can be incorporated into quantitative descriptions of community diversity, yet its use has been limited largely due to the difficulty in constructing phylogenies which incorporate the wide genomic diversity of microbial communities. Here, we describe the de...

Full description

Bibliographic Details
Main Authors: Xinyang Huang, David L. Erickson, Jianghong Meng
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.03455-22
_version_ 1811163396651876352
author Xinyang Huang
David L. Erickson
Jianghong Meng
author_facet Xinyang Huang
David L. Erickson
Jianghong Meng
author_sort Xinyang Huang
collection DOAJ
description ABSTRACT Phylogeny is a powerful tool that can be incorporated into quantitative descriptions of community diversity, yet its use has been limited largely due to the difficulty in constructing phylogenies which incorporate the wide genomic diversity of microbial communities. Here, we describe the development of a web portal, PhyloPlus, which enables users to generate customized phylogenies that may be applied to any bacterial or archaeal communities. We demonstrate the power of phylogeny by comparing metrics that employ phylogeny with those that do not when applied to data sets from two metagenomic studies (fermented food, n = 58; human microbiome, n = 60). This example shows how inclusion of all bacterial species identified by taxonomic classifiers (Kraken2 and Kaiju) made the phylogeny perfectly congruent to the corresponding classification outputs. Our phylogeny-based approach also enabled the construction of more constrained null models which (i) shed light into community structure and (ii) minimize potential inflation of type I errors. Construction of such null models allowed for the observation of under-dispersion in 44 (75.86%) food samples, with the metacommunity defined as bacteria that were found in different food matrices. We also observed that closely related species with high abundance and uneven distribution across different sites could potentially exaggerate the dissimilarity between phylogenetically similar communities if they were measured using traditional species-based metrics (Padj. = 0.003), whereas this effect was mitigated by incorporating phylogeny (Padj. = 1). In summary, our tool can provide additional insights into microbial communities of interest and facilitate the use of phylogeny-based approaches in metagenomic analyses. IMPORTANCE There has been an explosion of interest in how microbial diversity affects human health, food safety, and environmental functions among many other processes. Accurately measuring the diversity and structure of those communities is central to understanding their effects. Here, we describe the development of a freely available online tool, PhyloPlus, which allows users to generate custom phylogenies that may be applied to any data set, thereby removing a major obstacle to the application of phylogeny to metagenomic data analysis. We demonstrate that the genetic relatedness of the organisms within those communities is a critical feature of their overall diversity, and that using a phylogeny which captures and quantifies this diversity allows for much more accurate descriptions while preventing misleading conclusions based on estimates that ignore evolutionary relationships.
first_indexed 2024-04-10T06:44:34Z
format Article
id doaj.art-fa7109c457c541a2be1d8a2ec013fd2b
institution Directory Open Access Journal
issn 2150-7511
language English
last_indexed 2024-04-10T06:44:34Z
publishDate 2023-02-01
publisher American Society for Microbiology
record_format Article
series mBio
spelling doaj.art-fa7109c457c541a2be1d8a2ec013fd2b2023-02-28T14:06:24ZengAmerican Society for MicrobiologymBio2150-75112023-02-0114110.1128/mbio.03455-22PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic CommunitiesXinyang Huang0David L. Erickson1Jianghong Meng2Joint Institute for Food Safety and Applied Nutrition, Center for Food Safety Security Systems, University of Maryland, College Park, Maryland, USAJoint Institute for Food Safety and Applied Nutrition, Center for Food Safety Security Systems, University of Maryland, College Park, Maryland, USAJoint Institute for Food Safety and Applied Nutrition, Center for Food Safety Security Systems, University of Maryland, College Park, Maryland, USAABSTRACT Phylogeny is a powerful tool that can be incorporated into quantitative descriptions of community diversity, yet its use has been limited largely due to the difficulty in constructing phylogenies which incorporate the wide genomic diversity of microbial communities. Here, we describe the development of a web portal, PhyloPlus, which enables users to generate customized phylogenies that may be applied to any bacterial or archaeal communities. We demonstrate the power of phylogeny by comparing metrics that employ phylogeny with those that do not when applied to data sets from two metagenomic studies (fermented food, n = 58; human microbiome, n = 60). This example shows how inclusion of all bacterial species identified by taxonomic classifiers (Kraken2 and Kaiju) made the phylogeny perfectly congruent to the corresponding classification outputs. Our phylogeny-based approach also enabled the construction of more constrained null models which (i) shed light into community structure and (ii) minimize potential inflation of type I errors. Construction of such null models allowed for the observation of under-dispersion in 44 (75.86%) food samples, with the metacommunity defined as bacteria that were found in different food matrices. We also observed that closely related species with high abundance and uneven distribution across different sites could potentially exaggerate the dissimilarity between phylogenetically similar communities if they were measured using traditional species-based metrics (Padj. = 0.003), whereas this effect was mitigated by incorporating phylogeny (Padj. = 1). In summary, our tool can provide additional insights into microbial communities of interest and facilitate the use of phylogeny-based approaches in metagenomic analyses. IMPORTANCE There has been an explosion of interest in how microbial diversity affects human health, food safety, and environmental functions among many other processes. Accurately measuring the diversity and structure of those communities is central to understanding their effects. Here, we describe the development of a freely available online tool, PhyloPlus, which allows users to generate custom phylogenies that may be applied to any data set, thereby removing a major obstacle to the application of phylogeny to metagenomic data analysis. We demonstrate that the genetic relatedness of the organisms within those communities is a critical feature of their overall diversity, and that using a phylogeny which captures and quantifies this diversity allows for much more accurate descriptions while preventing misleading conclusions based on estimates that ignore evolutionary relationships.https://journals.asm.org/doi/10.1128/mbio.03455-22diversitymetagenomicsmicrobial genomicsmicrobiomephylogeny
spellingShingle Xinyang Huang
David L. Erickson
Jianghong Meng
PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
mBio
diversity
metagenomics
microbial genomics
microbiome
phylogeny
title PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
title_full PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
title_fullStr PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
title_full_unstemmed PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
title_short PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities
title_sort phyloplus a universal tool for phylogenetic interrogation of metagenomic communities
topic diversity
metagenomics
microbial genomics
microbiome
phylogeny
url https://journals.asm.org/doi/10.1128/mbio.03455-22
work_keys_str_mv AT xinyanghuang phyloplusauniversaltoolforphylogeneticinterrogationofmetagenomiccommunities
AT davidlerickson phyloplusauniversaltoolforphylogeneticinterrogationofmetagenomiccommunities
AT jianghongmeng phyloplusauniversaltoolforphylogeneticinterrogationofmetagenomiccommunities