An integrative framework of stochastic variational variable selection for joint analysis of multi-omics microbiome data

High-dimensional multi-omics microbiome data plays an important role in elucidating microbial communities’ interactions with their hosts and environment in critical diseases and ecological changes. Although Bayesian clustering methods have recently been used for the integrated analysis of multi-omics data, no method designed to analyze multi-omics microbiome data has been proposed. In this study, we propose a novel framework called integrative stochastic variational variable selection (I-SVVS), which is an extension of stochastic variational variable selection for high-dimensional microbiome data. The I-SVVS approach addresses a specific Bayesian mixture model for each type of omics data, such as an infinite Dirichlet multinomial mixture model for microbiome data and an infinite Gaussian mixture model for metabolomic data. This approach is expected to reduce the computational time of the clustering process and improve the accuracy of the clustering results. This method can also identify a critical set of representative variables in multi-omics micro-biome data. Three datasets from soybean, mice, and humans (each set integrated microbiome and metabolome) were used to demonstrate the potential of I-SVVS. The results suggest that I-SVVS achieved better accuracy and significantly faster computation than the existing methods in all cases of testing datasets and was able to identify the important microbiome species and metabolites that characterized a cluster.

[1]  N. Segata,et al.  Cardiometabolic health, diet and the gut microbiome: a meta-omics perspective , 2023, Nature Medicine.

[2]  S. Vernon,et al.  Multi-'omics of gut microbiome-host interactions in short- and long-term myalgic encephalomyelitis/chronic fatigue syndrome patients. , 2023, Cell host & microbe.

[3]  Yan Liu,et al.  Metabolite interactions between host and microbiota during health and disease: Which feeds the other? , 2023, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[4]  V. Copié,et al.  Gut microbiome dysbiosis drives metabolic dysfunction in Familial dysautonomia , 2023, Nature Communications.

[5]  M. Nold,et al.  Understanding respiratory microbiome–immune system interactions in health and disease , 2023, Science Translational Medicine.

[6]  Y. Ichihashi,et al.  High throughput method of 16S rRNA gene sequencing library preparation for plant root microbial community profiling , 2022, Scientific Reports.

[7]  C. Okafor,et al.  Bile acids and the gut microbiota: metabolic interactions and impacts on disease , 2022, Nature Reviews Microbiology.

[8]  Richard J. Giannone,et al.  Morphine and high-fat diet differentially alter the gut microbiota composition and metabolic function in lean versus obese mice , 2022, ISME Communications.

[9]  M. Burns,et al.  Identification of shared and disease-specific host gene–microbiome associations across human diseases using multi-omic integration , 2022, Nature Microbiology.

[10]  T. Fujiwara,et al.  Genomic Prediction of Green Fraction Dynamics in Soybean Using Unmanned Aerial Vehicles Observations , 2022, Frontiers in Plant Science.

[11]  L. Elo,et al.  Dirichlet process mixture models for single-cell RNA-seq clustering , 2022, Biology open.

[12]  X. Pang,et al.  Chronic intermittent hypoxia induces gut microbial dysbiosis and infers metabolic dysfunction in mice. , 2022, Sleep medicine.

[13]  A. Kurilshikov,et al.  Challenges and future directions for studying effects of host genetics on the gut microbiome , 2022, Nature Genetics.

[14]  Yong Bok Lee,et al.  Glutamic acid reshapes the plant microbiota to protect plants against pathogens , 2021, Microbiome.

[15]  Y. Ichihashi,et al.  Stochastic variational variable selection for high-dimensional microbiome data , 2021, bioRxiv.

[16]  T. Fujiwara,et al.  Time-series Multi-spectral Imaging in Soybean for Improving Biomass and Genomic Prediction Accuracy , 2021, bioRxiv.

[17]  O. Babalola,et al.  Metagenomic Analyses of Plant Growth-Promoting and Carbon-Cycling Genes in Maize Rhizosphere Soils with Distinct Land-Use and Management Histories , 2021, Genes.

[18]  P. Hirsch,et al.  Metagenomic approaches reveal differences in genetic diversity and relative abundance of nitrifying bacteria and archaea in contrasting soils , 2021, Scientific Reports.

[19]  Emmanuel O. Elijah,et al.  Intermittent Hypoxia and Hypercapnia Alter Diurnal Rhythms of Luminal Gut Microbiome and Metabolome , 2021, mSystems.

[20]  Emmanuel O. Elijah,et al.  Influence of Intermittent Hypoxia/Hypercapnia on Atherosclerosis, Gut Microbiome, and Metabolome , 2021, Frontiers in Physiology.

[21]  D. Coleman-Derr,et al.  Holo-omics for deciphering plant-microbiome interactions , 2021, Microbiome.

[22]  S. Isobe,et al.  Whole-genome sequence diversity and association analysis of 198 soybean accessions in mini-core collections , 2021, DNA research : an international journal for rapid publication of reports on genes and genomes.

[23]  Shiraz A. Shah,et al.  Large-scale association analyses identify host factors influencing human gut microbiome composition , 2020, Nature Genetics.

[24]  David A. Drew,et al.  Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals , 2021, Nature Medicine.

[25]  M. Hirai,et al.  Identification of a Unique Type of Isoflavone O-Methyltransferase, GmIOMT1, Based on Multi-Omics Analysis of Soybean under Biotic Stress , 2020, Plant & cell physiology.

[26]  S. Tringe,et al.  Plant–microbiome interactions: from community assembly to plant health , 2020, Nature Reviews Microbiology.

[27]  M. Kusano,et al.  Multi-omics analysis on an agroecosystem reveals the significant role of organic nitrogen to increase agricultural crop yield , 2020, Proceedings of the National Academy of Sciences.

[28]  Qun Ma,et al.  Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean , 2020, The ISME Journal.

[29]  Qun Ma,et al.  Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean , 2020, The ISME Journal.

[30]  A. Veilleux,et al.  Rapid and Concomitant Gut Microbiota and Endocannabinoidome Response to Diet-Induced Obesity in Mice , 2019, mSystems.

[31]  Joseph N. Paulson,et al.  Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome , 2019, Science.

[32]  B. Singh,et al.  Soil amendments with ethylene precursor alleviate negative impacts of salinity on soil microbial properties and productivity , 2019, Scientific Reports.

[33]  T. Spector,et al.  Interplay between the human gut microbiome and host metabolism , 2019, Nature Communications.

[34]  Mindaugas Margelevicius,et al.  A low‐complexity add‐on score for protein remote homology search with COMER , 2018, Bioinform..

[35]  Rob Knight,et al.  Intermittent Hypoxia and Hypercapnia, a Hallmark of Obstructive Sleep Apnea, Alters the Gut Microbiome and Metabolome , 2018, mSystems.

[36]  H. Toju,et al.  DNA metabarcoding of spiders, insects, and springtails for exploring potential linkage between above- and below-ground food webs , 2018, Zoological Letters.

[37]  Lorenz Wernisch,et al.  Clusternomics: Integrative context-dependent clustering for heterogeneous datasets , 2017, bioRxiv.

[38]  R. Farré,et al.  Chronic Sleep Disruption Alters Gut Microbiota, Induces Systemic and Adipose Tissue Inflammation and Insulin Resistance in Mice , 2016, Scientific Reports.

[39]  Mindaugas Margelevicius,et al.  Bayesian nonparametrics in protein remote homology search , 2016, Bioinform..

[40]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[41]  B. Glick,et al.  Bacterial Modulation of Plant Ethylene Levels , 2015, Plant Physiology.

[42]  Mark P. Waldrop,et al.  Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes , 2015, Nature.

[43]  J. Hamedi,et al.  Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria , 2015, Journal of Industrial Microbiology & Biotechnology.

[44]  J. Prosser,et al.  The Family Nitrosomonadaceae , 2014 .

[45]  A. Butte,et al.  The Integrative Human Microbiome Project: Dynamic Analysis of Microbiome-Host Omics Profiles during Periods of Human Health and Disease , 2014, Cell host & microbe.

[46]  A. Sugiyama,et al.  Changes in the Bacterial Community of Soybean Rhizospheres during Growth in the Field , 2014, PloS one.

[47]  Patrick D. Schloss,et al.  Microbiome Data Distinguish Patients with Clostridium difficile Infection and Non-C. difficile-Associated Diarrhea from Healthy Controls , 2014, mBio.

[48]  E. Kuramae,et al.  Taxonomical and functional microbial community selection in soybean rhizosphere , 2014, The ISME Journal.

[49]  Pelin Yilmaz,et al.  The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks , 2013, Nucleic Acids Res..

[50]  J. Clemente,et al.  Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice , 2013, Science.

[51]  Joshua M. Stuart,et al.  The Cancer Genome Atlas Pan-Cancer analysis project , 2013, Nature Genetics.

[52]  P. Mieczkowski,et al.  Practical innovations for high-throughput amplicon sequencing , 2013, Nature Methods.

[53]  L. McCue,et al.  Linking microbial community structure to β-glucosidic function in soil aggregates , 2013, The ISME Journal.

[54]  Masanori Arita,et al.  MRMPROBS: a data assessment and metabolite identification tool for large-scale multiple reaction monitoring based widely targeted metabolomics. , 2013, Analytical chemistry.

[55]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[56]  David B. Dunson,et al.  Bayesian consensus clustering , 2013, Bioinform..

[57]  C. Sander,et al.  Pattern discovery and cancer gene identification in integrated cancer genomic data , 2013, Proceedings of the National Academy of Sciences.

[58]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[59]  Chong Wang,et al.  Stochastic variational inference , 2012, J. Mach. Learn. Res..

[60]  C. Quince,et al.  Dirichlet Multinomial Mixtures: Generative Models for Microbial Metagenomics , 2012, PloS one.

[61]  K. Harada,et al.  Evaluation of soybean germplasm conserved in NIAS genebank and development of mini core collections , 2012, Breeding science.

[62]  Eric P. Xing,et al.  StructHDP: automatic inference of number of clusters and population structure from admixed genotype data , 2011, Bioinform..

[63]  Ruth Ley,et al.  Unravelling the effects of the environment and host genotype on the gut microbiome , 2011, Nature Reviews Microbiology.

[64]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[65]  M. Hirai,et al.  Widely Targeted Metabolomics Based on Large-Scale MS/MS Data for Elucidating Metabolite Accumulation Patterns in Plants , 2008, Plant & cell physiology.

[66]  A. Fukushima,et al.  High Impact Gene Discovery: Simple Strand-Specific mRNA Library Construction and Differential Regulatory Analysis Based on Gene Co-Expression Network. , 2018, Methods in molecular biology.

[67]  M. Pevsner-Fischer,et al.  The gut microbiome and hypertension , 2017, Current opinion in nephrology and hypertension.

[68]  M. Fishbein FAMILIAL DYSAUTONOMIA. , 1965, Postgraduate medicine.