Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut

Xiong, Weili; Morowitz, Michael J.; Banfield, Jillian F.

doi:10.1021/pr500936p

Title: Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut

Journal Article · Tue Oct 28 00:00:00 EDT 2014 · Journal of Proteome Research

DOI:https://doi.org/10.1021/pr500936p· OSTI ID:1185517

Xiong, Weili ^[1]; Morowitz, Michael J. ^[2]; Banfield, Jillian F. ^[3]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Pittsburgh, PA (United States). School of Medicine
Univ. of California, Berkeley, CA (United States)

The early-life microbiota establishment in the human infant gut is highly variable and plays a crucial role in host nutrients and immunity maturation. While high-performance mass spectrometry (MS)-based metaproteomics is a powerful method for the functional characterization of complex microbial communities, the construction of comprehensive metaproteomic information in human fecal samples is inhibited by the presence of abundant human proteins. To alleviate this restriction, we have designed a novel metaproteomic strategy based on Double Filtering (DF) to enhance microbial protein characterization in complex fecal samples from healthy premature infants. We improved the overall depth of infant gut proteome measurement, with an increase in the number of identified low abundance proteins, and observed greater than twofold improvement in metrics for microbial protein identifications and quantifications with a relatively high rank correlation to control. We further showed the substantial enhancement of this approach for extensively interpreting microbial functional categories between infants by affording more detailed and confident identified categories. This approach provided an avenue for in-depth measurement in the microbial component of infant fecal samples and thus comprehensive characterization of infant gut microbiome functionality.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1185517

Journal Information:: Journal of Proteome Research, Vol. 14, Issue 1; ISSN 1535-3893

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 53 works

Citation information provided by
Web of Science

References (32)

Diversity, stability and resilience of the human gut microbiota Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I. Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11550	journal	September 2012
The Impact of the Gut Microbiota on Human Health: An Integrative View Clemente, Jose C.; Ursell, Luke K.; Parfrey, Laura Wegener Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.01.035	journal	March 2012
The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models Nell, Sandra; Suerbaum, Sebastian; Josenhans, Christine Nature Reviews Microbiology, Vol. 8, Issue 8 https://doi.org/10.1038/nrmicro2403	journal	July 2010
Gut microbiota in obesity and metabolic disorders Sanz, Yolanda; Santacruz, Arlette; Gauffin, Paola Proceedings of the Nutrition Society, Vol. 69, Issue 3 https://doi.org/10.1017/S0029665110001813	journal	June 2010
Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination Berer, Kerstin; Mues, Marsilius; Koutrolos, Michail Nature, Vol. 479, Issue 7374 https://doi.org/10.1038/nature10554	journal	October 2011
Functional interactions between the gut microbiota and host metabolism Tremaroli, Valentina; Bäckhed, Fredrik Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11552	journal	September 2012
Host-Gut Microbiota Metabolic Interactions Nicholson, J. K.; Holmes, E.; Kinross, J. Science, Vol. 336, Issue 6086 https://doi.org/10.1126/science.1223813	journal	June 2012
The gut microbiota shapes intestinal immune responses during health and disease Round, June L.; Mazmanian, Sarkis K. Nature Reviews Immunology, Vol. 9, Issue 5 https://doi.org/10.1038/nri2515	journal	May 2009
Human nutrition, the gut microbiome and the immune system Kau, Andrew L.; Ahern, Philip P.; Griffin, Nicholas W. Nature, Vol. 474, Issue 7351 https://doi.org/10.1038/nature10213	journal	June 2011
Development of intestinal microbiota in infants and its impact on health Matamoros, Sebastien; Gras-Leguen, Christele; Le Vacon, Françoise Trends in Microbiology, Vol. 21, Issue 4 https://doi.org/10.1016/j.tim.2012.12.001	journal	April 2013
Convergent temporal dynamics of the human infant gut microbiota Trosvik, Pål; Stenseth, Nils Christian; Rudi, Knut The ISME Journal, Vol. 4, Issue 2 https://doi.org/10.1038/ismej.2009.96	journal	August 2009
Microbiota–immune system interaction: an uneasy alliance Salzman, Nita H. Current Opinion in Microbiology, Vol. 14, Issue 1 https://doi.org/10.1016/j.mib.2010.09.018	journal	February 2011
Redefining the Role of Intestinal Microbes in the Pathogenesis of Necrotizing Enterocolitis Morowitz, M. J.; Poroyko, V.; Caplan, M. PEDIATRICS, Vol. 125, Issue 4 https://doi.org/10.1542/peds.2009-3149	journal	March 2010
Bacterial colonization and gut development in preterm neonates Cilieborg, Malene S.; Boye, Mette; Sangild, Per T. Early Human Development, Vol. 88 https://doi.org/10.1016/j.earlhumdev.2011.12.027	journal	March 2012
Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns Dominguez-Bello, M. G.; Costello, E. K.; Contreras, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 26 https://doi.org/10.1073/pnas.1002601107	journal	June 2010
Life at the beginning: perturbation of the microbiota by antibiotics in early life and its role in health and disease Zeissig, Sebastian; Blumberg, Richard S. Nature Immunology, Vol. 15, Issue 4 https://doi.org/10.1038/ni.2847	journal	March 2014
Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa De Filippo, C.; Cavalieri, D.; Di Paola, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1005963107	journal	August 2010
Strain-resolved community genomic analysis of gut microbial colonization in a premature infant Morowitz, M. J.; Denef, V. J.; Costello, E. K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 3 https://doi.org/10.1073/pnas.1010992108	journal	December 2010
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Sharon, I.; Morowitz, M. J.; Thomas, B. C. Genome Research, Vol. 23, Issue 1 https://doi.org/10.1101/gr.142315.112	journal	August 2012
Metaproteomics : Harnessing the Power of High Performance Mass Spectrometry to Identify the Suite of Proteins That Control Metabolic Activities in Microbial Communities Hettich, Robert L.; Pan, Chongle; Chourey, Karuna Analytical Chemistry, Vol. 85, Issue 9 https://doi.org/10.1021/ac303053e	journal	March 2013
Systematic Comparison of Label-Free, Metabolic Labeling, and Isobaric Chemical Labeling for Quantitative Proteomics on LTQ Orbitrap Velos Li, Zhou; Adams, Rachel M.; Chourey, Karuna Journal of Proteome Research, Vol. 11, Issue 3 https://doi.org/10.1021/pr200748h	journal	January 2012
Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities Hettich, Robert L.; Sharma, Ritin; Chourey, Karuna Current Opinion in Microbiology, Vol. 15, Issue 3 https://doi.org/10.1016/j.mib.2012.04.008	journal	June 2012
Integrated Metagenomics/Metaproteomics Reveals Human Host-Microbiota Signatures of Crohn's Disease Erickson, Alison R.; Cantarel, Brandi L.; Lamendella, Regina PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049138	journal	November 2012
Shotgun metaproteomics of the human distal gut microbiota Verberkmoes, Nathan C.; Russell, Alison L.; Shah, Manesh The ISME Journal, Vol. 3, Issue 2 https://doi.org/10.1038/ismej.2008.108	journal	October 2008
Label-free Quantitative Proteomics for the Extremely Thermophilic Bacterium Caldicellulosiruptor obsidiansis Reveal Distinct Abundance Patterns upon Growth on Cellobiose, Crystalline Cellulose, and Switchgrass Lochner, Adriane; Giannone, Richard J.; Keller, Martin Journal of Proteome Research, Vol. 10, Issue 12 https://doi.org/10.1021/pr200536j	journal	December 2011
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Defining the Boundaries and Characterizing the Landscape of Functional Genome Expression in Vascular Tissues of Populus using Shotgun Proteomics Abraham, Paul; Adams, Rachel; Giannone, Richard J. Journal of Proteome Research, Vol. 11, Issue 1 https://doi.org/10.1021/pr200851y	journal	November 2011
WebMGA: a customizable web server for fast metagenomic sequence analysis Wu, Sitao; Zhu, Zhengwei; Fu, Liming BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-444	journal	September 2011
A computational method for assessing peptide- identification reliability in tandem mass spectrometry analysis with SEQUEST Razumovskaya, Jane; Olman, Victor; Xu, Dong PROTEOMICS, Vol. 4, Issue 4 https://doi.org/10.1002/pmic.200300656	journal	April 2004
ScanRanker: Quality Assessment of Tandem Mass Spectra via Sequence Tagging Ma, Ze-Qiang; Chambers, Matthew C.; Ham, Amy-Joan L. Journal of Proteome Research, Vol. 10, Issue 7 https://doi.org/10.1021/pr200118r	journal	July 2011

Cited By (20)

metaQuantome: An Integrated, Quantitative Metaproteomics Approach Reveals Connections Between Taxonomy and Protein Function in Complex Microbiomes Easterly, Caleb W.; Sajulga, Ray; Mehta, Subina Molecular & Cellular Proteomics, Vol. 18, Issue 8 suppl 1 https://doi.org/10.1074/mcp.ra118.001240	journal	June 2019
Proteomic Stable Isotope Probing Reveals Biosynthesis Dynamics of Slow Growing Methane Based Microbial Communities Marlow, Jeffrey J.; Skennerton, Connor T.; Li, Zhou Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00563	journal	April 2016
Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life Xiong, Weili; Brown, Christopher T.; Morowitz, Michael J. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0290-6	journal	July 2017
A decade of metaproteomics: Where we stand and what the future holds: PROTEOMICS Wilmes, Paul; Heintz-Buschart, Anna; Bond, Philip L. PROTEOMICS, Vol. 15, Issue 20 https://doi.org/10.1002/pmic.201500183	journal	September 2015
Metaproteomic and 16S rRNA Gene Sequencing Analysis of the Infant Fecal Microbiome Cortes, Laetitia; Wopereis, Harm; Tartiere, Aude International Journal of Molecular Sciences, Vol. 20, Issue 6 https://doi.org/10.3390/ijms20061430	journal	March 2019
More Is Not Always Better: Evaluation of 1D and 2D-LC-MS/MS Methods for Metaproteomics Hinzke, Tjorven; Kouris, Angela; Hughes, Rebecca-Ayme Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00238	journal	February 2019
Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mbio.00530-17	journal	August 2017
Proteogenomics Reveals Novel Reductive Dehalogenases and Methyltransferases Expressed during Anaerobic Dichloromethane Metabolism Kleindienst, Sara; Chourey, Karuna; Chen, Gao Applied and Environmental Microbiology, Vol. 85, Issue 6 https://doi.org/10.1128/aem.02768-18	journal	January 2019
Challenges in Clinical Metaproteomics Highlighted by the Analysis of Acute Leukemia Patients with Gut Colonization by Multidrug-Resistant Enterobacteriaceae Rechenberger, Julia; Samaras, Patroklos; Jarzab, Anna Proteomes, Vol. 7, Issue 1 https://doi.org/10.3390/proteomes7010002	journal	January 2019
Metaproteomic and Metabolomic Approaches for Characterizing the Gut Microbiome Peters, Danielle L.; Wang, Wenju; Zhang, Xu PROTEOMICS, Vol. 19, Issue 16 https://doi.org/10.1002/pmic.201800363	journal	July 2019
Metaproteomic strategies and applications for gut microbial research Xiao, Mingming; Yang, Junjun; Feng, Yuxin Applied Microbiology and Biotechnology, Vol. 101, Issue 8 https://doi.org/10.1007/s00253-017-8215-7	journal	March 2017
Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02129	journal	September 2018
The Microbiome: The Trillions of Microorganisms That Maintain Health and Cause Disease in Humans and Companion Animals Hoffmann, A. Rodrigues; Proctor, L. M.; Surette, M. G. Veterinary Pathology, Vol. 53, Issue 1 https://doi.org/10.1177/0300985815595517	journal	July 2015
Metaproteomics as a Complementary Approach to Gut Microbiota in Health and Disease Petriz, Bernardo A.; Franco, Octávio L. Frontiers in Chemistry, Vol. 5 https://doi.org/10.3389/fchem.2017.00004	journal	January 2017
Integrated multi-omics of the human gut microbiome in a case study of familial type 1 diabetes Heintz-Buschart, Anna; May, Patrick; Laczny, Cédric C. Nature Microbiology, Vol. 2, Issue 1 https://doi.org/10.1038/nmicrobiol.2016.180	journal	October 2016
Chronic kidney disease and the gut microbiome Hobby, Gerren P.; Karaduta, Oleg; Dusio, Giuseppina F. American Journal of Physiology-Renal Physiology, Vol. 316, Issue 6 https://doi.org/10.1152/ajprenal.00298.2018	journal	June 2019
MetaLab 2.0 Enables Accurate Post-Translational Modifications Profiling in Metaproteomics Cheng, Kai; Ning, Zhibin; Zhang, Xu Journal of the American Society for Mass Spectrometry, Vol. 31, Issue 7 https://doi.org/10.1021/jasms.0c00083	journal	May 2020
Erratum for Skennerton et al., “Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea” Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder mBio, Vol. 8, Issue 5 https://doi.org/10.1128/mbio.01561-17	journal	November 2017
Metaproteomic analysis of human gut microbiota: where are we heading? Lee, Pey Yee; Chin, Siok-Fong; Neoh, Hui-min Journal of Biomedical Science, Vol. 24, Issue 1 https://doi.org/10.1186/s12929-017-0342-z	journal	June 2017
A Quantitative Proteomics Approach to Clinical Research with Non-Traditional Samples Licier, Rígel; Miranda, Eric; Serrano, Horacio Proteomes, Vol. 4, Issue 4 https://doi.org/10.3390/proteomes4040031	journal	October 2016

Similar Records

Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life

Journal Article · Mon Jul 10 00:00:00 EDT 2017 · Microbiome · OSTI ID:1185517

Xiong, Weili; Brown, Christopher T.; Morowitz, Michael J.; +2 more

Antibiotic resistance and host immune system-induced metal bactericidal control are key factors for microbial persistence in the developing human preterm infant gut microbiome

Journal Article · Mon Nov 21 00:00:00 EST 2022 · Frontiers in Microbiology · OSTI ID:1185517

Peters, Samantha L.; Morowitz, Michael J.; Hettich, Robert L.

Metaproteomics reveals persistent and phylum-redundant metabolic functional stability in adult human gut microbiomes of Crohn’s remission patients despite temporal variations in microbial taxa, genomes, and proteomes

Journal Article · Mon Feb 11 00:00:00 EST 2019 · Microbiome · OSTI ID:1185517

Blakeley-Ruiz, J. Alfredo; Erickson, Alison R.; Cantarel, Brandi L.; +5 more

Related Subjects

60 APPLIED LIFE SCIENCES
Metaproteome
human infant gut
shotgun proteomics
double filtering

Title: Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut

Citation Formats

References (32)

Cited By (20)

Similar Records

Related Subjects