Deciphering functional redundancy in the human microbiome

被引:135
|
作者
Tian, Liang [1 ,2 ,3 ,4 ,5 ]
Wang, Xu-Wen [1 ,2 ]
Wu, Ang-Kun [1 ,2 ,6 ]
Fan, Yuhang [1 ,2 ,7 ]
Friedman, Jonathan [8 ]
Dahlin, Amber [1 ,2 ]
Waldor, Matthew K. [2 ,9 ,10 ]
Weinstock, George M. [11 ]
Weiss, Scott T. [1 ,2 ]
Liu, Yang-Yu [1 ,2 ]
机构
[1] Brigham & Womens Hosp, Channing Div Network Med, 75 Francis St, Boston, MA 02115 USA
[2] Harvard Med Sch, Boston, MA 02115 USA
[3] Hong Kong Baptist Univ, Dept Phys, Hong Kong, Peoples R China
[4] Hong Kong Baptist Univ, Inst Computat & Theoret Studies, Hong Kong, Peoples R China
[5] Hong Kong Baptist Univ, State Key Lab Environm & Biol Anal, Hong Kong, Peoples R China
[6] Rutgers State Univ, Dept Phys & Astron, Piscataway, NJ 08854 USA
[7] Stanford Univ, Dept Bioengn, Stanford, CA 94305 USA
[8] Hebrew Univ Jerusalem, Fac Agr Food & Environm, Dept Plant Pathol & Microbiol, Jerusalem, Israel
[9] Brigham & Womens Hosp, Div Infect Dis, 75 Francis St, Boston, MA 02115 USA
[10] Howard Hughes Med Inst, Boston, MA 02115 USA
[11] Jackson Lab Genom Med, Farmington, CT 06117 USA
基金
美国国家卫生研究院;
关键词
GUT MICROBIOTA; RESILIENCE; DIVERSITY; STABILITY; RESOURCE; DATABASE; SUBSETS; STRAINS; GENOMES; OBESE;
D O I
10.1038/s41467-020-19940-1
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved - implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stability and resilience of the human microbiome, but this hypothesis has never been quantitatively tested. The origin of functional redundancy is still elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network - a bipartite graph that links microbes to the genes in their genomes. We find that this network exhibits several topological features that favor high functional redundancy. Furthermore, we develop a simple genome evolution model to generate genomic content network, finding that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with key topological features that favor high functional redundancy. Finally, we analyze data from two published studies of fecal microbiota transplantation (FMT), finding that high functional redundancy of the recipient's pre-FMT microbiota raises barriers to donor microbiota engraftment. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience. Here, the authors develop a genome evolution model to investigate the origin of functional redundancy in the human microbiome by analyzing its genomic content network and illustrate potential ecological and evolutionary processes that may contribute to its resilience.
引用
收藏
页数:11
相关论文
共 50 条
  • [1] Deciphering functional redundancy in the human microbiome
    Liang Tian
    Xu-Wen Wang
    Ang-Kun Wu
    Yuhang Fan
    Jonathan Friedman
    Amber Dahlin
    Matthew K. Waldor
    George M. Weinstock
    Scott T. Weiss
    Yang-Yu Liu
    [J]. Nature Communications, 11
  • [2] Deciphering functional redundancy and energetics of malate oxidation in mycobacteria
    Harold, Liam K.
    Jinich, Adrian
    Hards, Kiel
    Cordeiro, Alexandra
    Keighley, Laura M.
    Cross, Alec
    McNeil, Matthew B.
    Rhee, Kyu
    Cook, Gregory M.
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2022, 298 (05)
  • [3] Deciphering the Chemistry of the Human Gut Microbiome
    Balskus, Emily P.
    [J]. CHEMISTRY OF MICROBIOMES, 2017, : 57 - 63
  • [4] Behind Taxonomic Variability: The Functional Redundancy in the Tick Microbiome
    Estrada-Pena, Agustin
    Cabezas-Cruz, Alejandro
    Obregon, Dasiel
    [J]. MICROORGANISMS, 2020, 8 (11) : 1 - 16
  • [5] Deciphering the human gut microbiome with chemistry.
    Balskus, Emily P.
    [J]. CANCER RESEARCH, 2020, 80 (08) : 23 - 23
  • [6] Deciphering the Functional Redundancy of USP4 and USP15
    Zachariah, S.
    Coulombe, J.
    Zhang, M.
    Gray, D.
    [J]. JOURNAL OF THORACIC ONCOLOGY, 2020, 15 (02) : S20 - S21
  • [7] Deciphering the impacts of gut and tissue microbiome on human cancers
    Godbole, Mukul S.
    Singh, Vishal
    [J]. CANCER REPORTS, 2023, 6 (11)
  • [8] Operons and the effect of genome redundancy in deciphering functional relationships using phylogenetic profiles
    Moreno-Hagelsieb, Gabriel
    Janga, Sarath Chandra
    [J]. PROTEINS-STRUCTURE FUNCTION AND BIOINFORMATICS, 2008, 70 (02) : 344 - 352
  • [9] Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics
    Leyuan Li
    Tong Wang
    Zhibin Ning
    Xu Zhang
    James Butcher
    Joeselle M. Serrana
    Caitlin M. A. Simopoulos
    Janice Mayne
    Alain Stintzi
    David R. Mack
    Yang-Yu Liu
    Daniel Figeys
    [J]. Nature Communications, 14
  • [10] Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics
    Li, Leyuan
    Wang, Tong
    Ning, Zhibin
    Zhang, Xu
    Butcher, James
    Serrana, Joeselle M. M.
    Simopoulos, Caitlin M. A.
    Mayne, Janice
    Stintzi, Alain
    Mack, David R. R.
    Liu, Yang-Yu
    Figeys, Daniel
    [J]. NATURE COMMUNICATIONS, 2023, 14 (01)