Bacterial census of poultry intestinal microbiome

doi:10.3382/PS.2012-02822

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Bacterial census of poultry intestinal microbiome

Journal Article•DOI•

Bacterial census of poultry intestinal microbiome

Shan Wei¹, Mark Morrison¹, Mark Morrison², Zhongtang Yu¹•Institutions (2)

Ohio State University¹, Commonwealth Scientific and Industrial Research Organisation²

01 Mar 2013-Poultry Science (Oxford University Press)-Vol. 92, Iss: 3, pp 671-683

TL;DR: A phylogenetic diversity census of bacteria identified in the intestinal tract of chickens and turkeys using a naïve analysis of all the curated 16S rRNA gene sequences archived in public databases helps identify gaps in knowledge on bacterial diversity in poultry gastrointestinal tract.

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About: This article is published in Poultry Science.The article was published on 2013-03-01 and is currently open access. It has received 356 citations till now. The article focuses on the topics: Phylogenetic diversity & Bacterial phyla.

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Journal Article•DOI•

Impact of Heat Stress on Poultry Production

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Lucas J. Lara¹, Marcos H. Rostagno²•Institutions (2)

Purdue University¹, Agricultural Research Service²

24 Apr 2013-Animal

TL;DR: Further research is still needed to improve the knowledge of basic mechanisms associated to the negative effects of heat stress in poultry, as well as to develop effective interventions to deal with heat stress conditions.

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Abstract: Understanding and controlling environmental conditions is crucial to successful poultry production and welfare. Heat stress is one of the most important environmental stressors challenging poultry production worldwide. The detrimental effects of heat stress on broilers and laying hens range from reduced growth and egg production to decreased poultry and egg quality and safety. Moreover, the negative impact of heat stress on poultry welfare has recently attracted increasing public awareness and concern. Much information has been published on the effects of heat stress on productivity and immune response in poultry. However, our knowledge of basic mechanisms associated to the reported effects, as well as related to poultry behavior and welfare under heat stress conditions is in fact scarce. Intervention strategies to deal with heat stress conditions have been the focus of many published studies. Nevertheless, effectiveness of most of the interventions has been variable or inconsistent. This review focuses on the scientific evidence available on the importance and impact of heat stress in poultry production, with emphasis on broilers and laying hens.

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774 citations

Cites background from "Bacterial census of poultry intesti..."

...The intestinal tract of poultry harbors a complex and dynamic microbial ecosystem (or microbiome), which may be affected by a variety of factors [84]....
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Journal Article•DOI•

Intestinal microbiome of poultry and its interaction with host and diet.

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Deng Pan, Zhongtang Yu¹•Institutions (1)

Ohio State University¹

01 Jan 2014-Gut microbes

TL;DR: A comprehensive understanding of these interactions will help develop new dietary or managerial interventions that can enhance bird growth, maximize host feed utilization, and protect birds from enteric diseases caused by pathogenic bacteria.

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Abstract: The gastrointestinal (GI) tract of poultry is densely populated with microorganisms which closely and intensively interact with the host and ingested feed. The gut microbiome benefits the host by providing nutrients from otherwise poorly utilized dietary substrates and modulating the development and function of the digestive and immune system. In return, the host provides a permissive habitat and nutrients for bacterial colonization and growth. Gut microbiome can be affected by diet, and different dietary interventions are used by poultry producers to enhance bird growth and reduce risk of enteric infection by pathogens. There also exist extensive interactions among members of the gut microbiome. A comprehensive understanding of these interactions will help develop new dietary or managerial interventions that can enhance bird growth, maximize host feed utilization, and protect birds from enteric diseases caused by pathogenic bacteria.

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555 citations

Cites background or methods from "Bacterial census of poultry intesti..."

...com Gut Microbes 109 Sequencing of 16S rRNA genes by first the Sanger sequencing technology and recently next-generation sequencing (NGS) technologies make it possible to comprehensively characterize the intestinal microbiome of poultry, and the sequence information has greatly expanded our knowledge on the bacterial diversity present in the intestinal tract, particularly the cecum, of chickens and turkeys.(2) Through phylogenetic and statistical analysis of 16S rRNA gene sequences recovered from intestinal microbiome of both chickens and turkeys, a global bacterial census was created for poultry intestinal microbiome....
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...Through phylogenetic and statistical analysis of 16S rRNA gene sequences recovered from intestinal microbiome of both chickens and turkeys, a global bacterial census was created for poultry intestinal microbiome.(2) Although this census is not complete, it serves as a phylogenetic framework for the bacterial diversity in the intestinal microbiome of both chickens and turkeys....
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...The cecum of both chickens and turkeys harbors a complex microbiome, which is almost exclusively composed of bacteria.(2) Early cultivation-based studies revealed low abundances of lactobacilli (>10(4)/g colony forming units, CFUs) and clostridia (10(2)–10(4)/g CFUs) in the small intestines and high abundance (10(10)–10(11)/g microscope counts) of anaerobic bacteria in the cecum of chickens....
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Journal Article•DOI•

The chicken gastrointestinal microbiome

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Brian B. Oakley¹, Brian B. Oakley², Hyun S. Lillehoj², Michael H. Kogut², Woo Kyun Kim³, John J. Maurer³, A. A. Pedroso³, Margie D. Lee³, Stephen R. Collett³, Timothy J. Johnson⁴, Nelson A. Cox² - Show less +7 more•Institutions (4)

Western University of Health Sciences¹, Agricultural Research Service², University of Georgia³, University of Minnesota⁴

01 Nov 2014-Fems Microbiology Letters

TL;DR: An overview of the current state of knowledge of the chicken gastrointestinal microbiome focusing on spatial and temporal variability, the presence and importance of human pathogens, the influence of the microbiota on the immune system, and the importance of the microbiome for poultry nutrition is provided.

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Abstract: The domestic chicken is a common model organism for human biological research and of course also forms the basis of a global protein industry. Recent methodological advances have spurred the recognition of microbiomes as complex communities with important influences on the health and disease status of the host. In this minireview, we provide an overview of the current state of knowledge of the chicken gastrointestinal microbiome focusing on spatial and temporal variability, the presence and importance of human pathogens, the influence of the microbiota on the immune system, and the importance of the microbiome for poultry nutrition. Review and meta-analysis of public data showed cecal communities dominated by Firmicutes and Bacteroides at the phylum level, while at finer levels of taxonomic resolution, a phylogenetically diverse assemblage of microorganisms appears to have similar metabolic functions that provide important benefits to the host as inferred from metagenomic data. This observation of functional redundancy may have important implications for management of the microbiome. We foresee advances in strategies to improve gut health in commercial operations through management of the intestinal microbiota as an alternative to in-feed subtherapeutic antibiotics, improvements in pre- and probiotics, improved management of polymicrobial poultry diseases, and better control of human pathogens via colonization reduction or competitive exclusion strategies.

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468 citations

Additional excerpts

...Data from Wei et al. (2013) represent publically...
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Journal Article•DOI•

Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease.

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Dragana Stanley¹, Dragana Stanley², Robert J. Hughes³, Robert J. Hughes¹, Robert J. Hughes⁴, Robert J. Moore¹ - Show less +2 more•Institutions (4)

University of New England (United States)¹, Central Queensland University², University of Adelaide³, South Australian Research and Development Institute⁴

19 Mar 2014-Applied Microbiology and Biotechnology

TL;DR: This review aims to address the main issues in investigating chicken microbiota and to summarise the data acquired to date.

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Abstract: Recent advances in the technology available for culture-independent methods for identification and enumeration of environmental bacteria have invigorated interest in the study of the role of chicken intestinal microbiota in health and productivity. Chickens harbour unique and diverse bacterial communities that include human and animal pathogens. Increasing public concern about the use of antibiotics in the poultry industry has influenced the ways in which poultry producers are working towards improving birds' intestinal health. Effective means of antibiotic-independent pathogen control through competitive exclusion and promotion of good protective microbiota are being actively investigated. With the realisation that just about any change in environment influences the highly responsive microbial communities and with the abandonment of the notion that we can isolate and investigate a single species of interest outside of the community, came a flood of studies that have attempted to profile the intestinal microbiota of chickens under numerous conditions. This review aims to address the main issues in investigating chicken microbiota and to summarise the data acquired to date.

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395 citations

Cites background from "Bacterial census of poultry intesti..."

...The chicken GIT harbours a very diverse microbiota that aids in the breakdown and digestion of food and comprised over 900 species of bacteria (Apajalahti et al. 2004; Wei et al. 2013)....
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Journal Article•DOI•

Extensive Microbial and Functional Diversity within the Chicken Cecal Microbiome

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Martin J. Sergeant¹, Chrystala Constantinidou¹, Tristan A Cogan², Michael R. Bedford³, Charles W. Penn⁴, Mark J. Pallen¹ - Show less +2 more•Institutions (4)

University of Warwick¹, University of Bristol², AmeriCorps VISTA³, University of Birmingham⁴

21 Mar 2014-PLOS ONE

TL;DR: The cecal metagenome encodes several fermentation pathways leading to the production of short-chain fatty acids, including some with novel features, and it is speculated that these provide major hydrogen sinks within this microbial community and might explain the high abundance of several genera within this microbiome.

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Abstract: Chickens are major source of food and protein worldwide. Feed conversion and the health of chickens relies on the largely unexplored complex microbial community that inhabits the chicken gut, including the ceca. We have carried out deep microbial community profiling of the microbiota in twenty cecal samples via 16S rRNA gene sequences and an in-depth metagenomics analysis of a single cecal microbiota. We recovered 699 phylotypes, over half of which appear to represent previously unknown species. We obtained 648,251 environmental gene tags (EGTs), the majority of which represent new species. These were binned into over two-dozen draft genomes, which included Campylobacter jejuni and Helicobacter pullorum. We found numerous polysaccharide- and oligosaccharide-degrading enzymes encoding within the metagenome, some of which appeared to be part of polysaccharide utilization systems with genetic evidence for the co-ordination of polysaccharide degradation with sugar transport and utilization. The cecal metagenome encodes several fermentation pathways leading to the production of short-chain fatty acids, including some with novel features. We found a dozen uptake hydrogenases encoded in the metagenome and speculate that these provide major hydrogen sinks within this microbial community and might explain the high abundance of several genera within this microbiome, including Campylobacter, Helicobacter and Megamonas.

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335 citations

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References

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Open Access

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Journal Article•DOI•

The neighbor-joining method: a new method for reconstructing phylogenetic trees.

[...]

Naruya Saitou¹, Masatoshi Nei•Institutions (1)

University of Texas Health Science Center at Houston¹

01 Jul 1987-Molecular Biology and Evolution

TL;DR: The neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods for reconstructing phylogenetic trees from evolutionary distance data.

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Abstract: A new method called the neighbor-joining method is proposed for reconstructing phylogenetic trees from evolutionary distance data. The principle of this method is to find pairs of operational taxonomic units (OTUs [= neighbors]) that minimize the total branch length at each stage of clustering of OTUs starting with a starlike tree. The branch lengths as well as the topology of a parsimonious tree can quickly be obtained by using this method. Using computer simulation, we studied the efficiency of this method in obtaining the correct unrooted tree in comparison with that of five other tree-making methods: the unweighted pair group method of analysis, Farris's method, Sattath and Tversky's method, Li's method, and Tateno et al.'s modified Farris method. The new, neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods.

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57,055 citations

"Bacterial census of poultry intesti..." refers methods in this paper

...To generate a detailed phylogenetic tree using the neighbor-joining method (Saitou and Nei, 1987), the resultant aligned sequences were inserted into the Silva ARB tree constructed from the Silva reference data set, with each sequence being inserted into a branch with which the sequence had the…...
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...…nih.gov/), Silva comprehensive ribosomal RNA database (Silva, http://www.arb-silva.de/), and Ribosomal Database Project (RDP, http://rdp.cme.msu.edu/) in January and February, 2012, using the following search terms: chicken, chickens, chick, chicks, poultry, broiler, hen, hens, turkey, and turkeys....
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Journal Article•DOI•

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

[...]

Patrick D. Schloss¹, Patrick D. Schloss², Sarah L. Westcott¹, Sarah L. Westcott², Thomas Ryabin¹, Justine R. Hall³, Martin Hartmann⁴, Emily B. Hollister⁵, Ryan A. Lesniewski⁶, Brian B. Oakley⁷, Donovan H. Parks⁸, Courtney J. Robinson², Jason W. Sahl⁹, Blaz Stres¹⁰, Gerhard G. Thallinger¹¹, David J. Van Horn², Carolyn F. Weber¹² - Show less +13 more•Institutions (12)

University of Massachusetts Amherst¹, University of Michigan², University of New Mexico³, University of British Columbia⁴, Texas A&M University⁵, University of Minnesota⁶, University of Warwick⁷, Dalhousie University⁸, Colorado School of Mines⁹, University of Ljubljana¹⁰, Graz University of Technology¹¹, Louisiana State University¹²

01 Dec 2009-Applied and Environmental Microbiology

TL;DR: M mothur is used as a case study to trim, screen, and align sequences; calculate distances; assign sequences to operational taxonomic units; and describe the α and β diversity of eight marine samples previously characterized by pyrosequencing of 16S rRNA gene fragments.

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Abstract: mothur aims to be a comprehensive software package that allows users to use a single piece of software to analyze community sequence data. It builds upon previous tools to provide a flexible and powerful software package for analyzing sequencing data. As a case study, we used mothur to trim, screen, and align sequences; calculate distances; assign sequences to operational taxonomic units; and describe the alpha and beta diversity of eight marine samples previously characterized by pyrosequencing of 16S rRNA gene fragments. This analysis of more than 222,000 sequences was completed in less than 2 h with a laptop computer.

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17,350 citations

Journal Article•DOI•

Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy

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Qiong Wang, George M. Garrity¹, James M. Tiedje¹, James R. Cole•Institutions (1)

Michigan State University¹

15 Aug 2007-Applied and Environmental Microbiology

TL;DR: The RDP Classifier can rapidly and accurately classify bacterial 16S rRNA sequences into the new higher-order taxonomy proposed in Bergey's Taxonomic Outline of the Prokaryotes, and the majority of the classification errors appear to be due to anomalies in the current taxonomies.

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Abstract: The Ribosomal Database Project (RDP) Classifier, a naive Bayesian classifier, can rapidly and accurately classify bacterial 16S rRNA sequences into the new higher-order taxonomy proposed in Bergey's Taxonomic Outline of the Prokaryotes (2nd ed., release 5.0, Springer-Verlag, New York, NY, 2004). It provides taxonomic assignments from domain to genus, with confidence estimates for each assignment. The majority of classifications (98%) were of high estimated confidence (≥95%) and high accuracy (98%). In addition to being tested with the corpus of 5,014 type strain sequences from Bergey's outline, the RDP Classifier was tested with a corpus of 23,095 rRNA sequences as assigned by the NCBI into their alternative higher-order taxonomy. The results from leave-one-out testing on both corpora show that the overall accuracies at all levels of confidence for near-full-length and 400-base segments were 89% or above down to the genus level, and the majority of the classification errors appear to be due to anomalies in the current taxonomies. For shorter rRNA segments, such as those that might be generated by pyrosequencing, the error rate varied greatly over the length of the 16S rRNA gene, with segments around the V2 and V4 variable regions giving the lowest error rates. The RDP Classifier is suitable both for the analysis of single rRNA sequences and for the analysis of libraries of thousands of sequences. Another related tool, RDP Library Compare, was developed to facilitate microbial-community comparison based on 16S rRNA gene sequence libraries. It combines the RDP Classifier with a statistical test to flag taxa differentially represented between samples. The RDP Classifier and RDP Library Compare are available online at http://rdp.cme.msu.edu/.

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16,048 citations

"Bacterial census of poultry intesti..." refers methods in this paper

...To minimize fragment effect of sequences corresponding to different regions of 16S rRNA gene, the aligned sequences were first clustered based on the Silva bacterial sequence templates using the Cluster.fragment function of Mothur (Schloss et al., 2009)....
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...Possible chimeric sequences were identified using Chimera Slayer and UCHIME in the Mothur package (Schloss et al., 2009; Edgar et al., 2011; Haas et al., 2011) and removed....
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...The intestinal microbiomes of chickens and turkeys were compared using 3 methods: weighted UniFrac distance, which measures the phylogenetic distance between sets of taxa as phylogenetic trees (Lozupone and Knight, 2005; Lemos et al., 2012); the SONS function in the Mothur package, which compares 2 microbiomes by taking into consideration of OTU richness, membership, and structure (Schloss and Handelsman, 2006; Schloss et al., 2009); and Krona charts that allows comparison between micobiomes based on detailed phylogenetic composition....
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...When compared with respect to OTU richness, membership, and structure using the SONS function within the Mothur program, the Yue-Clayton similarity index (θyc, ranging from 0 for 2 completely different communities to 1 for 2 identical communities; Yue and Clayton, 2005) was only 0.16 at species-equivalent level and 0.59 at phylum level, indicating 2 distinct intestinal microbiomes (Table 2)....
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...Based on the classifications determined by the Classifier program in Mothur (Wang et al., 2007; Schloss et al., 2009), distance matrices were computed within ARB software (Ludwig et al., 2004) with the Jukes-Cantor correction applied for the following bacterial groups: total bacteria, the phylum Bacteroidetes, the phylum Firmicutes, the phylum Proteobacteria, and sequences of cecum origin....
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Journal Article•DOI•

UCHIME improves sensitivity and speed of chimera detection

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Robert C. Edgar, Brian J. Haas¹, Jose C. Clemente¹, Christopher Quince¹, Rob Knight¹ - Show less +1 more•Institutions (1)

University of Colorado Boulder¹

01 Aug 2011-Bioinformatics

TL;DR: UCHIME has better sensitivity than ChimeraSlayer (previously the most sensitive database method), especially with short, noisy sequences, and in testing on artificial bacterial communities with known composition, UCHIME de novo sensitivity is shown to be comparable to Perseus.

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Abstract: Motivation: Chimeric DNA sequences often form during polymerase chain reaction amplification, especially when sequencing single regions (e.g. 16S rRNA or fungal Internal Transcribed Spacer) to assess diversity or compare populations. Undetected chimeras may be misinterpreted as novel species, causing inflated estimates of diversity and spurious inferences of differences between populations. Detection and removal of chimeras is therefore of critical importance in such experiments. Results: We describe UCHIME, a new program that detects chimeric sequences with two or more segments. UCHIME either uses a database of chimera-free sequences or detects chimeras de novo by exploiting abundance data. UCHIME has better sensitivity than ChimeraSlayer (previously the most sensitive database method), especially with short, noisy sequences. In testing on artificial bacterial communities with known composition, UCHIME de novo sensitivity is shown to be comparable to Perseus. UCHIME is >100× faster than Perseus and >1000× faster than ChimeraSlayer. Contact: [email protected] Availability: Source, binaries and data: http://drive5.com/uchime. Supplementary information:Supplementary data are available at Bioinformatics online.

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11,904 citations

"Bacterial census of poultry intesti..." refers methods in this paper

...Possible chimeric sequences were identified using Chimera Slayer and UCHIME in the Mothur package (Schloss et al., 2009; Edgar et al., 2011; Haas et al., 2011) and removed....
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Journal Article•DOI•

ARB: a software environment for sequence data

[...]

Wolfgang Ludwig¹, Oliver Strunk, Ralf Westram, Lothar Richter, Harald Meier, Yadhukumar², Arno Buchner, Tina Lai, Susanne Steppi, Gangolf Jobb, Wolfram Förster, Igor Brettske, Stefan Gerber, Anton W. Ginhart, Oliver Gross, Silke Grumann, Stefan Hermann, Ralf Jost, Andreas König, Thomas Liss, Ralph Lüßmann, Michael May, Björn Nonhoff, Boris Reichel, Robert Strehlow, Alexandros Stamatakis, Norbert Stuckmann, Alexander Vilbig, Michael Lenke¹, Thomas Ludwig¹, Arndt Bode, Karl-Heinz Schleifer - Show less +28 more•Institutions (2)

Technische Universität München¹, Max Planck Society²

15 Mar 2004-Nucleic Acids Research

TL;DR: The ARB program package comprises a variety of directly interacting software tools for sequence database maintenance and analysis which are controlled by a common graphical user interface.

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Abstract: The ARB (from Latin arbor, tree) project was initiated almost 10 years ago. The ARB program package comprises a variety of directly interacting software tools for sequence database maintenance and analysis which are controlled by a common graphical user interface. Although it was initially designed for ribosomal RNA data, it can be used for any nucleic and amino acid sequence data as well. A central database contains processed (aligned) primary structure data. Any additional descriptive data can be stored in database fields assigned to the individual sequences or linked via local or worldwide networks. A phylogenetic tree visualized in the main window can be used for data access and visualization. The package comprises additional tools for data import and export, sequence alignment, primary and secondary structure editing, profile and filter calculation, phylogenetic analyses, specific hybridization probe design and evaluation and other components for data analysis. Currently, the package is used by numerous working groups worldwide.

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6,757 citations

"Bacterial census of poultry intesti..." refers methods in this paper

...To generate a detailed phylogenetic tree using the neighbor-joining method (Saitou and Nei, 1987), the resultant aligned sequences were inserted into the Silva ARB tree constructed from the Silva reference data set, with each sequence being inserted into a branch with which the sequence had the…...
[...]
...22) with the Silva SSU_Ref_NR_108 data set (Ludwig et al., 2004) as reference sequences (Schloss et al., 2009)....
[...]
...…determined by the Classifier program in Mothur (Wang et al., 2007; Schloss et al., 2009), distance matrices were computed within ARB software (Ludwig et al., 2004) with the Jukes-Cantor correction applied for the following bacterial groups: total bacteria, the phylum Bacteroidetes, the…...
[...]
...The 16S rRNA gene sequences of chicken and turkey origin were retrieved from the 3 public databases of nucleic acids including GenBank (http://www.ncbi.nlm. nih.gov/), Silva comprehensive ribosomal RNA database (Silva, http://www.arb-silva.de/), and Ribosomal Database Project (RDP,…...
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