Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant

Brooks, Brandon; Mueller, R. S.; Young, Jacque C.; Morowitz, Michael J.; Banfield, Jillian F.

doi:10.3389/fmicb.2015.00654

Title: Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant

Journal Article · Wed Jul 01 00:00:00 EDT 2015 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2015.00654· OSTI ID:1265682

Brooks, Brandon ^[1]; Mueller, R. S. ^[2]; Young, Jacque C. ^[3]; Morowitz, Michael J. ^[4]; Banfield, Jillian F. ^[1]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Oregon State Univ., Corvallis, OR (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Pittsburgh School of Medicine, Pittsburgh, PA (United States)

While there has been growing interest in the gut microbiome in recent years, it remains unclear whether closely related species and strains have similar or distinct functional roles and if organisms capable of both aerobic and anaerobic growth do so simultaneously. To investigate these questions, we implemented a high-throughput mass spectrometry-based proteomics approach to identify proteins in fecal samples collected on days of life 13 21 from an infant born at 28 weeks gestation. No prior studies have coupled strain-resolved community metagenomics to proteomics for such a purpose. Sequences were manually curated to resolve the genomes of two strains of Citrobacter that were present during the later stage of colonization. Proteome extracts from fecal samples were processed via a nano-2D-LC-MS/MS and peptides were identified based on information predicted from the genome sequences for the dominant organisms, Serratia and the two Citrobacter strains. These organisms are facultative anaerobes, and proteomic information indicates the utilization of both aerobic and anaerobic metabolisms throughout the time series. This may indicate growth in distinct niches within the gastrointestinal tract. We uncovered differences in the physiology of coexisting Citrobacter strains, including differences in motility and chemotaxis functions. Additionally, for both Citrobacter strains we resolved a community-essential role in vitamin metabolism and a predominant role in propionate production. Finally, in this case study we detected differences between genome abundance and activity levels for the dominant populations. This underlines the value in layering proteomic information over genetic potential.

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:: 1265682

Journal Information:: Frontiers in Microbiology, Vol. 6, Issue 1; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 22 works

Citation information provided by
Web of Science

References (42)

Differences of small intestinal bacteria populations in adults and children with/without celiac disease: Effect of age, gluten diet, and disease Nistal, Esther; Caminero, Alberto; Herrán, Alexandra R. Inflammatory Bowel Diseases, Vol. 18, Issue 4 https://doi.org/10.1002/ibd.21830	journal	April 2012
Trimethylamine N-oxide: role in cell senescence and age-related diseases Zhang, Lin; Yu, Fang; Xia, Jian European Journal of Nutrition https://doi.org/10.1007/s00394-022-03011-w	journal	October 2022
Binning Metagenomic Contigs Using Unsupervised Clustering and Reference Databases Jiang, Zhongjun; Li, Xiaobo; Guo, Lijun Interdisciplinary Sciences: Computational Life Sciences, Vol. 14, Issue 4 https://doi.org/10.1007/s12539-022-00526-y	journal	May 2022
Tit-for-Tat: Type VI Secretion System Counterattack during Bacterial Cell-Cell Interactions Basler, Marek; Ho, Brian T.; Mekalanos, John J. Cell, Vol. 152, Issue 4 https://doi.org/10.1016/j.cell.2013.01.042	journal	February 2013
Microbiota Modulate Behavioral and Physiological Abnormalities Associated with Neurodevelopmental Disorders Hsiao, Elaine Y.; McBride, Sara W.; Hsien, Sophia Cell, Vol. 155, Issue 7 https://doi.org/10.1016/j.cell.2013.11.024	journal	December 2013
Concurrent Bloodstream Infections in Infants with Necrotizing Enterocolitis Bizzarro, Matthew J.; Ehrenkranz, Richard A.; Gallagher, Patrick G. The Journal of Pediatrics, Vol. 164, Issue 1 https://doi.org/10.1016/j.jpeds.2013.09.020	journal	January 2014
Microbial adhesins to gastrointestinal mucus Juge, Nathalie Trends in Microbiology, Vol. 20, Issue 1 https://doi.org/10.1016/j.tim.2011.10.001	journal	January 2012
Bacterial microcompartments and the modular construction of microbial metabolism Kerfeld, Cheryl A.; Erbilgin, Onur Trends in Microbiology, Vol. 23, Issue 1 https://doi.org/10.1016/j.tim.2014.10.003	journal	January 2015
Analysis of Quantitative Proteomic Data Generated via Multidimensional Protein Identification Technology Washburn, Michael P.; Ulaszek, Ryan; Deciu, Cosmin Analytical Chemistry, Vol. 74, Issue 7 https://doi.org/10.1021/ac015704l	journal	April 2002
The dynamics of gut-associated microbial communities during inflammation Winter, Sebastian E.; Lopez, Christopher A.; Bäumler, Andreas J. EMBO reports, Vol. 14, Issue 4 https://doi.org/10.1038/embor.2013.27	journal	March 2013
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
An obesity-associated gut microbiome with increased capacity for energy harvest Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A. Nature, Vol. 444, Issue 7122 https://doi.org/10.1038/nature05414	journal	December 2006
Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria Lo, Ian; Denef, Vincent J.; VerBerkmoes, Nathan C. Nature, Vol. 446, Issue 7135 https://doi.org/10.1038/nature05624	journal	March 2007
Swimming against the tide: progress and challenges in our understanding of colicin translocation Kleanthous, Colin Nature Reviews Microbiology, Vol. 8, Issue 12 https://doi.org/10.1038/nrmicro2454	journal	November 2010
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
Correlation Between Intraluminal Oxygen Gradient and Radial Partitioning of Intestinal Microbiota Albenberg, Lindsey; Esipova, Tatiana V.; Judge, Colleen P. Gastroenterology, Vol. 147, Issue 5 https://doi.org/10.1053/j.gastro.2014.07.020	journal	November 2014
The role of the intestinal microcirculation in necrotizing enterocolitis Watkins, Daniel J.; Besner, Gail E. Seminars in Pediatric Surgery, Vol. 22, Issue 2 https://doi.org/10.1053/j.sempedsurg.2013.01.004	journal	May 2013
Succession of microbial consortia in the developing infant gut microbiome Koenig, J. E.; Spor, A.; Scalfone, N. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000081107	journal	July 2010
Additional maternal and nonmaternal factors contribute to microbiota shaping in newborns Putignani, Lorenza; Carsetti, Rita; Signore, Fabrizio Proceedings of the National Academy of Sciences, Vol. 107, Issue 42 https://doi.org/10.1073/pnas.1010526107	journal	September 2010
Normal gut microbiota modulates brain development and behavior Heijtz, R. D.; Wang, S.; Anuar, F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1010529108	journal	January 2011
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
Relating the metatranscriptome and metagenome of the human gut Franzosa, E. A.; Morgan, X. C.; Segata, N. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1319284111	journal	May 2014
The ENZYME database in 2000 Bairoch, A. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.304	journal	January 2000
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
Inositol Supplementation in Premature Infants with Respiratory Distress Syndrome Hallman, M.; Bry, K.; Hoppu, K. Retina, Vol. 13, Issue 1 https://doi.org/10.1097/00006982-199313010-00019	journal	January 1993
Carbon and electron flow in Clostridium butyricum grown in chemostat culture on glycerol and on glucose Abbad-Andaloussi, S.; Durr, C.; Raval, G. Microbiology, Vol. 142, Issue 5 https://doi.org/10.1099/13500872-142-5-1149	journal	May 1996
Altered colonic function and microbiota profile in a mouse model of chronic depression Park, A. J.; Collins, J.; Blennerhassett, P. A. Neurogastroenterology & Motility, Vol. 25, Issue 9 https://doi.org/10.1111/nmo.12153	journal	June 2013
Community Proteomics of a Natural Microbial Biofilm Ram, Rachna J.; VerBerkmoes, Nathan C.; Thelen, Michael P. Science, Vol. 308, Issue 5730 https://doi.org/10.1126/science.1109070	journal	June 2005
Gut Microbiomes of Malawian Twin Pairs Discordant for Kwashiorkor Smith, Michelle I.; Yatsunenko, Tanya; Manary, Mark J. Science, Vol. 339, Issue 6119 https://doi.org/10.1126/science.1229000	journal	January 2013
Adaptive and Mutational Resistance: Role of Porins and Efflux Pumps in Drug Resistance Fernandez, L.; Hancock, R. E. W. Clinical Microbiology Reviews, Vol. 25, Issue 4 https://doi.org/10.1128/cmr.00043-12	journal	October 2012
Curli Biogenesis and Function Barnhart, Michelle M.; Chapman, Matthew R. Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142106	journal	October 2006
Strainer: software for analysis of population variation in community genomic datasets Eppley, John M.; Tyson, Gene W.; Getz, Wayne M. BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-398	journal	October 2007
Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants Brooks, Brandon; Firek, Brian A.; Miller, Christopher S. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-1	journal	January 2014
Development of the preterm infant gut microbiome: a research priority Groer, Maureen W.; Luciano, Angel A.; Dishaw, Larry J. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-38	journal	January 2014
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
Meconium Microbiome Analysis Identifies Bacteria Correlated with Premature Birth Ardissone, Alexandria N.; de la Cruz, Diomel M.; Davis-Richardson, Austin G. PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0090784	journal	March 2014
How delivery mode and feeding can shape the bacterial community in the infant gut Song, S. J.; Dominguez-Bello, M. G.; Knight, R. Canadian Medical Association Journal, Vol. 185, Issue 5 https://doi.org/10.1503/cmaj.130147	journal	February 2013
Factors Influencing the Composition of the Intestinal Microbiota in Early Infancy Penders, J.; Thijs, C.; Vink, C. PEDIATRICS, Vol. 118, Issue 2 https://doi.org/10.1542/peds.2005-2824	journal	August 2006
Type VI Secretion: Not Just for Pathogenesis Anymore A., Cotter, Peggy; J., Jani, Andrea The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/bcp2-ma26	text	January 2010
Effect of Breast and Formula Feeding on Gut Microbiota Shaping in Newborns Guaraldi, Federica; Salvatori, Guglielmo Frontiers in Cellular and Infection Microbiology, Vol. 2 https://doi.org/10.3389/fcimb.2012.00094	journal	January 2012
The Human Neonatal Gut Microbiome: A Brief Review Gritz, Emily C.; Bhandari, Vineet Frontiers in Pediatrics, Vol. 3 https://doi.org/10.3389/fped.2015.00017	journal	March 2015
Role of the gut microbiota in inflammatory bowel disease pathogenesis: What have we learnt in the past 10 years? Hold, Georgina L. World Journal of Gastroenterology, Vol. 20, Issue 5 https://doi.org/10.3748/wjg.v20.i5.1192	journal	January 2014

Cited By (9)

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
Gut microbial functional maturation and succession during human early life Cerdó, Tomás; Ruiz, Alicia; Acuña, Inmaculada Environmental Microbiology, Vol. 20, Issue 6 https://doi.org/10.1111/1462-2920.14235	journal	May 2018
Meta-proteomic analysis of protein expression distinctive to electricity-generating biofilm communities in air-cathode microbial fuel cells Chignell, Jeremy F.; De Long, Susan K.; Reardon, Kenneth F. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1111-2	journal	April 2018
The impact of sequence database choice on metaproteomic results in gut microbiota studies Tanca, Alessandro; Palomba, Antonio; Fraumene, Cristina Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0196-8	journal	September 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
Estimating relative biomasses of organisms in microbiota using “phylopeptidomics” Pible, Olivier; Allain, François; Jouffret, Virginie Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00797-x	journal	March 2020
Monitoring Perinatal Gut Microbiota in Mouse Models by Mass Spectrometry Approaches: Parental Genetic Background and Breastfeeding Effects Levi Mortera, Stefano; Del Chierico, Federica; Vernocchi, Pamela Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01523	journal	September 2016
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2687	journal	January 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:1265682

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

Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles

Journal Article · Tue Apr 10 00:00:00 EDT 2018 · mBio (Online) · OSTI ID:1265682

Brown, Christopher T.; Xiong, Weili; Olm, Matthew R.; +6 more

Knock-out of SO1377 gene, which encodes the member of a conserved hypothetical bacterial protein family COG2268, results in alteration of iron metabolism, increased spontaneous mutation and hydrogen peroxide sensitivity in Shewanella oneidensis MR-1

Journal Article · Thu Apr 06 00:00:00 EDT 2006 · BMC Genomics · OSTI ID:1265682

Gao, Weimin; Liu, Yongqing; Giometti, Carol S.; +6 more

Related Subjects

60 APPLIED LIFE SCIENCES
colonization
infant gut
metaproteomics
microbiome
microbial ecology
physiology

Title: Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant

Citation Formats

References (42)

Cited By (9)

Similar Records

Related Subjects