skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach

Abstract

Investigations of gut microbiomes have shed light on the diversity and genetic content of these communities, and helped shape our understanding of how host-associated microorganisms influence host physiology, behavior, and health. Despite the importance of gut microbes to metazoans, our understanding of the changes in diversity and composition across the alimentary tract, and the source of the resident community are limited. Here, using community metagenomics and 16S rRNA gene sequencing, we assess microbial community diversity and coding potential in the foregut, midgut, and hindgut of a juvenile Panchlora cockroach, which resides in the refuse piles of the leaf-cutter ant species Atta colombica. We found a significant shift in the microbial community structure and coding potential throughout the three gut sections of Panchlora sp., and through comparison with previously generated metagenomes of the cockroach's food source and niche, we reveal that this shift in microbial community composition is influenced by the ecosystems in which Panchlora sp. occurs. While the foregut is composed of microbes that likely originate from the symbiotic fungus gardens of the ants, the midgut and hindgut are composed of a microbial community that is likely cockroach-specific. Analogous to mammalian systems, the midgut and hindgut appear to be dominatedmore » by Firmicutes and Bacteroidetes with the capacity for polysaccharide degradation, suggesting they may assist in the degradation of dietary plant material. Our work underscores the prominence of community changes throughout gut microbiomes and highlights ecological factors that underpin the structure and function of the symbiotic microbial communities of metazoans.« less

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1357714
Alternate Identifier(s):
OSTI ID: 1379830
Grant/Contract Number:  
AC02-05CH11231; FC02-07ER64494; FC02- 07ER64494
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 12 Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Gontang, Erin A., Aylward, Frank O., Carlos, Camila, Glavina del Rio, Tijana, Chovatia, Mansi, Fern, Alison, Lo, Chien-Chi, Malfatti, Stephanie A., Tringe, Susannah G., Currie, Cameron R., Kolter, Roberto, and Appanna, ed., Vasu D. Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0177189.
Gontang, Erin A., Aylward, Frank O., Carlos, Camila, Glavina del Rio, Tijana, Chovatia, Mansi, Fern, Alison, Lo, Chien-Chi, Malfatti, Stephanie A., Tringe, Susannah G., Currie, Cameron R., Kolter, Roberto, & Appanna, ed., Vasu D. Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach. United States. doi:10.1371/journal.pone.0177189.
Gontang, Erin A., Aylward, Frank O., Carlos, Camila, Glavina del Rio, Tijana, Chovatia, Mansi, Fern, Alison, Lo, Chien-Chi, Malfatti, Stephanie A., Tringe, Susannah G., Currie, Cameron R., Kolter, Roberto, and Appanna, ed., Vasu D. Thu . "Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach". United States. doi:10.1371/journal.pone.0177189.
@article{osti_1357714,
title = {Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach},
author = {Gontang, Erin A. and Aylward, Frank O. and Carlos, Camila and Glavina del Rio, Tijana and Chovatia, Mansi and Fern, Alison and Lo, Chien-Chi and Malfatti, Stephanie A. and Tringe, Susannah G. and Currie, Cameron R. and Kolter, Roberto and Appanna, ed., Vasu D.},
abstractNote = {Investigations of gut microbiomes have shed light on the diversity and genetic content of these communities, and helped shape our understanding of how host-associated microorganisms influence host physiology, behavior, and health. Despite the importance of gut microbes to metazoans, our understanding of the changes in diversity and composition across the alimentary tract, and the source of the resident community are limited. Here, using community metagenomics and 16S rRNA gene sequencing, we assess microbial community diversity and coding potential in the foregut, midgut, and hindgut of a juvenile Panchlora cockroach, which resides in the refuse piles of the leaf-cutter ant species Atta colombica. We found a significant shift in the microbial community structure and coding potential throughout the three gut sections of Panchlora sp., and through comparison with previously generated metagenomes of the cockroach's food source and niche, we reveal that this shift in microbial community composition is influenced by the ecosystems in which Panchlora sp. occurs. While the foregut is composed of microbes that likely originate from the symbiotic fungus gardens of the ants, the midgut and hindgut are composed of a microbial community that is likely cockroach-specific. Analogous to mammalian systems, the midgut and hindgut appear to be dominated by Firmicutes and Bacteroidetes with the capacity for polysaccharide degradation, suggesting they may assist in the degradation of dietary plant material. Our work underscores the prominence of community changes throughout gut microbiomes and highlights ecological factors that underpin the structure and function of the symbiotic microbial communities of metazoans.},
doi = {10.1371/journal.pone.0177189},
journal = {PLoS ONE},
number = 5,
volume = 12,
place = {United States},
year = {2017},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pone.0177189

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores
journal, July 2010

  • Pope, P. B.; Denman, S. E.; Jones, M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 33
  • DOI: 10.1073/pnas.1005297107

Host-specific assemblages typify gut microbial communities of related insect species
journal, March 2014


The Pfam protein families database
journal, December 2007

  • Finn, R. D.; Tate, J.; Mistry, J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm960

Rumen bacterial diversity as determined by sequence analysis of 16S rDNA libraries
journal, June 1999


KAAS: an automatic genome annotation and pathway reconstruction server
journal, May 2007

  • Moriya, Y.; Itoh, M.; Okuda, S.
  • Nucleic Acids Research, Vol. 35, Issue S2, p. W182-W185
  • DOI: 10.1093/nar/gkm321

Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-Cutter Ants
journal, November 2009


Mountain Pine Beetles Colonizing Historical and Naïve Host Trees Are Associated with a Bacterial Community Highly Enriched in Genes Contributing to Terpene Metabolism
journal, March 2013

  • Adams, Aaron S.; Aylward, Frank O.; Adams, Sandye M.
  • Applied and Environmental Microbiology, Vol. 79, Issue 11
  • DOI: 10.1128/AEM.00068-13

Metagenomic Analysis of the Human Distal Gut Microbiome
journal, June 2006


Host-Bacterial Mutualism in the Human Intestine
journal, March 2005


Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont
journal, October 2009

  • Sabree, Z. L.; Kambhampati, S.; Moran, N. A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 46
  • DOI: 10.1073/pnas.0907504106

Microbial Ecology of the Cockroach Gut
journal, October 1987


The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Microbiome of Fungus-Growing Termites: a New Reservoir for Lignocellulase Genes
journal, November 2010

  • Liu, Ning; Yan, Xing; Zhang, Meiling
  • Applied and Environmental Microbiology, Vol. 77, Issue 1
  • DOI: 10.1128/AEM.01521-10

Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows
journal, September 2011

  • Godoy-Vitorino, Filipa; Goldfarb, Katherine C.; Karaoz, Ulas
  • The ISME Journal, Vol. 6, Issue 3
  • DOI: 10.1038/ismej.2011.131

MetaGene: prokaryotic gene finding from environmental genome shotgun sequences
journal, October 2006

  • Noguchi, Hideki; Park, Jungho; Takagi, Toshihisa
  • Nucleic Acids Research, Vol. 34, Issue 19
  • DOI: 10.1093/nar/gkl723

The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data
journal, January 2007

  • Cole, J. R.; Chai, B.; Farris, R. J.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl889

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

Evidence of cellulose metabolism by the giant panda gut microbiome
journal, October 2011

  • Zhu, L.; Wu, Q.; Dai, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 43
  • DOI: 10.1073/pnas.1017956108

Complementary symbiont contributions to plant decomposition in a fungus-farming termite
journal, September 2014

  • Poulsen, Michael; Hu, Haofu; Li, Cai
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 40
  • DOI: 10.1073/pnas.1319718111

Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
journal, October 2014

  • Aylward, Frank O.; Suen, Garret; Biedermann, Peter H. W.
  • mBio, Vol. 5, Issue 6
  • DOI: 10.1128/mBio.02077-14

Human distal gut microbiome: Human microbiome
journal, September 2011


The Human Gut Microbiome: Ecology and Recent Evolutionary Changes
journal, October 2011


Obesity alters gut microbial ecology
journal, July 2005

  • Ley, R. E.; Backhed, F.; Turnbaugh, P.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 31
  • DOI: 10.1073/pnas.0504978102

Microbial Community Structure of Leaf-Cutter Ant Fungus Gardens and Refuse Dumps
journal, March 2010


The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants
journal, January 2012


Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models
journal, August 2009

  • Brady, Arthur; Salzberg, Steven L.
  • Nature Methods, Vol. 6, Issue 9
  • DOI: 10.1038/nmeth.1358

T HE G UT B ACTERIA OF I NSECTS : Nonpathogenic Interactions
journal, January 2004


Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples
journal, January 2012


Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis
journal, June 2011


Role of Microorganisms in the Digestion of Lignocellulose by Termites
journal, January 1994


IMG/M: a data management and analysis system for metagenomes
journal, December 2007

  • Markowitz, V. M.; Ivanova, N. N.; Szeto, E.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm869

Blattabacteria, the endosymbionts of cockroaches, have small genome sizes and high genome copy numbers
journal, December 2008


Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera
journal, September 2001

  • Nalepa, C. A.; Bignell, D. E.; Bandi, C.
  • Insectes Sociaux, Vol. 48, Issue 3
  • DOI: 10.1007/PL00001767

Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases
journal, January 2009

  • Brulc, Jennifer M.; Antonopoulos, Dionysios A.; Berg Miller, Margret E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 6
  • DOI: 10.1073/pnas.0806191105

Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts
journal, April 1998

  • Leadbetter, Jared R.; Crosby, Laurel D.; Breznak, J. A.
  • Archives of Microbiology, Vol. 169, Issue 4
  • DOI: 10.1007/s002030050574

Symbiotic digestion of lignocellulose in termite guts
journal, February 2014


Functional diversity within the simple gut microbiota of the honey bee
journal, June 2012

  • Engel, P.; Martinson, V. G.; Moran, N. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1202970109

Diversity and Genomes of Uncultured Microbial Symbionts in the Termite Gut
journal, June 2010

  • Hongoh, Yuichi
  • Bioscience, Biotechnology, and Biochemistry, Vol. 74, Issue 6
  • DOI: 10.1271/bbb.100094

The Bacterial Community in the Gut of the Cockroach Shelfordella lateralis Reflects the Close Evolutionary Relatedness of Cockroaches and Termites
journal, February 2012

  • Schauer, Christine; Thompson, Claire L.; Brune, Andreas
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.07788-11

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Evidence for Cocladogenesis Between Diverse Dictyopteran Lineages and Their Intracellular Endosymbionts
journal, April 2003


Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite
journal, November 2007

  • Warnecke, Falk; Luginbühl, Peter; Ivanova, Natalia
  • Nature, Vol. 450, Issue 7169
  • DOI: 10.1038/nature06269

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches
journal, June 2000


An obesity-associated gut microbiome with increased capacity for energy harvest
journal, December 2006

  • Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A.
  • Nature, Vol. 444, Issue 7122
  • DOI: 10.1038/nature05414

Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria
journal, March 2009


Time Required for Food Passage through the Alimentary Tract of the Cockroach, Periplaneta Americana Linn.
journal, June 1937

  • Snipes, B. Thomas; Tauber, Oscar E.
  • Annals of the Entomological Society of America, Vol. 30, Issue 2
  • DOI: 10.1093/aesa/30.2.277

Bacterial biogeography of the human digestive tract
journal, November 2011

  • Stearns, Jennifer C.; Lynch, Michael D. J.; Senadheera, Dilani B.
  • Scientific Reports, Vol. 1, Issue 1
  • DOI: 10.1038/srep00170

An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity
journal, September 2010


MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013

  • Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
  • Molecular Biology and Evolution, Vol. 30, Issue 12
  • DOI: 10.1093/molbev/mst197

IMG ER: a system for microbial genome annotation expert review and curation
journal, June 2009


Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011


Human gut microbes associated with obesity
journal, December 2006

  • Ley, Ruth E.; Turnbaugh, Peter J.; Klein, Samuel
  • Nature, Vol. 444, Issue 7122
  • DOI: 10.1038/4441022a

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens
journal, March 2012

  • Aylward, Frank O.; Burnum, Kristin E.; Scott, Jarrod J.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.10