Cited by 1,121Gut microbiota and healthRuminant Nutrition and Digestive PhysiologyAnimal Nutrition and Physiology

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Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP)

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Dowd, Scot E, Callaway, Todd R, Wolcott, Randall D, Sun, Yan, McKeehan, Trevor, Hagevoort, Robert G, Edrington, Thomas S·2008·BMC Microbiology

DOI 10.1186/1471-2180-8-125PMC PMC2515157

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Abstract

BACKGROUND: The microbiota of an animal's intestinal tract plays important roles in the animal's overall health, productivity and well-being. There is still a scarcity of information on the microbial diversity in the gut of livestock species such as cattle. The primary reason for this lack of data relates to the expense of methods needed to generate such data. Here we have utilized a bacterial tag-encoded FLX 16s rDNA amplicon pyrosequencing (bTEFAP) approach that is able to perform diversity analyses of gastrointestinal populations. bTEFAP is relatively inexpensive in terms of both time and labor due to the implementation of a novel tag priming method and an efficient bioinformatics pipeline. We have evaluated the microbiome from the feces of 20 commercial, lactating dairy cows. RESULTS: Ubiquitous bacteria detected from the cattle feces included Clostridium, Bacteroides, Porpyhyromonas, Ruminococcus, Alistipes, Lachnospiraceae, Prevotella, Lachnospira, Enterococcus, Oscillospira, Cytophage, Anaerotruncus, and Acidaminococcus spp. Foodborne pathogenic bacteria were detected in several of the cattle, a total of 4 cows were found to be positive for Salmonella spp (tentative enterica) and 6 cows were positive for Campylobacter spp. (tentative lanienae). CONCLUSION: Using bTEFAP we have examined the microbiota in the feces of cattle. As these methods continue to mature we will better understand the ecology of the major populations of bacteria the lower intestinal tract. This in turn will allow for a better understanding of ways in which the intestinal microbiome contributes to animal health, productivity and wellbeing.

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Temporal changes in the bacterial community of animal feces and their correlation with stable fly oviposition, larval development, and adult fitness
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Complexity, Temporal Stability, and Clinical Correlates of Airway Bacterial Community Composition in Primary Ciliary Dyskinesia
Rogers, G. B., Carroll, M. P., Zain, N. M. M., Bruce, K. D., Lock, K., Walker, W. T., Jones, G., Daniels, T. W. V., & Lucas, J. S. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.02164-13 · Cited by 52
Main microorganisms involved in the fermentation of Ugandan ghee
Ongol, M. P., & Asano, K. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.06.003 · Cited by 51
“Clostridium is highly prevalent in dairy faecal343 samples and constitutes 20% of the total microbial population (Dowd et al., 2008).”
BackgroundMethod
Examination of protein degradation in continuous flow, microbial electrolysis cells treating fermentation wastewater
Nam, J.-Y., Yates, M. D., Zaybak, Z., & Logan, B. E. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.08.065 · Cited by 51
Changes in bacterial community metabolism and composition during the degradation of dissolved organic matter from the jellyfish Aurelia aurita in a Mediterranean coastal lagoon
Blanchet, M., Pringault, O., Bouvy, M., Catala, P., Oriol, L., Caparros, J., Ortega‐Retuerta, E., Intertaglia, L., West, N. J., Agis, M., et al. (2014) · Environmental Science and Pollution Research · doi:10.1007/s11356-014-3848-x · Cited by 52
In Silico and Experimental Evaluation of Primer Sets for Species-Level Resolution of the Vaginal Microbiota Using 16S Ribosomal RNA Gene Sequencing
Pol, W. J. V. D., Kumar, R., Morrow, C. D., Blanchard, E., Taylor, C. M., Martin, D. H., Lefkowitz, E. J., & Muzny, C. A. (2018) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiy508 · Cited by 51
“V1–V3 Commonly used universal 28F [33] 519R [34] 5ʹ-GAGTTTGATCNTGGCTCAG-3ʹ 5ʹ-GTNTCACNGCGGCKKGCTG-3ʹ Vaginal microbiome study Fwd-P1 Fwd-P2 Rev1B [17] 5ʹ-GTTYGATYMTGGCTYAG-3ʹ5ʹ-RTTTGATCYTGGTTCAG-3ʹ 5ʹ-ATTACCGCGGCTGCTGG-3ʹ V3–V4 Commonly used universal 357wF [35] 785R [35] 5ʹ-CCTACGGGNGGCWGCAG-3ʹ 5ʹ-GACTACHVGGGTWTCTAAT…”
Bacterial communities associated to Chilean altiplanic native plants from the Andean grasslands soils
Fernández-Gómez, B., Maldonado, J. E., Mandaković, D., Gaete, A., Gutiérrez, R. A., Maass, A., Cambiazo, V., & González, M. (2019) · Scientific Reports · doi:10.1038/s41598-018-37776-0 · Cited by 50
Microbial diversity of eolian dust sources from saline lake sediments and biological soil crusts in arid Southern Australia
Abed, R. M. M., Ramette, A., Hübner, V., Patrick De Deckker, B., & de Beer, D. (2012) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2011.01289.x · Cited by 50
Bacterial community dynamics in surface flow constructed wetlands for the treatment of swine waste
Ibekwe, A. M., Ma, J., Murinda, S. E., & Reddy, G. B. (2015) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2015.11.139 · Cited by 50
“The genus Bacteroides is enriched within the gut microbiota of many mammals (Dowd et al., 2008; Fogarty and Voytek, 2005; Juteau et al., 2005) and specific species within this order have been proposed as fecal indicators (Weary et al., 2008).”
Background
Archaeal and bacterial community dynamics and bioprocess performance of a bench-scale two-stage anaerobic digester
González‐Martínez, A., García-Ruiz, M. J., Rodríguez–Sánchez, A., Osorio, F., & González-López, J. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7393-z · Cited by 50
“2007) were used for the archaeal 16S rRNA gene amplification and the primers 530F (5′-GTGCCAGCMGCNGCGG3′) and 1100R (5′-GGGTTNCGNTCGTTG-3′) (Dowd et al. 2008) were used for the amplification of the 16S rRNA gene of the domain Bacteria.”
Method
Yeast fermentate prebiotic improves intestinal barrier integrity during heat stress by modulation of the gut microbiota in rats
Ducray, H. A. G., Globa, L. P., Pustovyy, O. M., Morrison, E. E., Vodyanoy, V. J., & Sorokulova, I. B. (2019) · Journal of Applied Microbiology · doi:10.1111/jam.14361 · Cited by 52
“Amplicon sequencing using next generation technology (bTEFAP) was originally described by Dowd et al. (2008).”
Method
Capturing Greater 16S rRNA Gene Sequence Diversity within the Domain Bacteria
Winsley, T. J., van Dorst, J. M., Brown, M. V., & Ferrari, B. C. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.01299-12 · Cited by 49
“Subsequently, the primer pair was validated in triplicate by bar-coded amplicon pyrosequencing on a Roche 454 Titanium instrument (Roche, Branford, CT) (7).”
Method
Effect of antimicrobial growth promoter administration on the intestinal microbiota of beef cattle
Reti, K. L., Thomas, M. C., Yanke, L., Selinger, L., & Inglis, G. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-8 · Cited by 43
“Almost all characterizations of the intestinal microbiota of cattle utilizing molecular methods to date have focused on the examination of fecal matter [21-23].”
Background
Culture Independent Survey of the Microbiota of the Glassy-Winged Sharpshooter (Homalodisca vitripennis) Using 454 Pyrosequencing
Hail, D., Lauzìere, I., Dowd, S. E., & Bextine, B. R. (2011) · Environmental Entomology · doi:10.1603/en10115 · Cited by 49
Soil characterisation by bacterial community analysis for forensic applications: A quantitative comparison of environmental technologies
Habtom, H. T., Demanèche, S., Dawson, L., Azulay, C., Matan, O., Robe, P., Gafny, R., Simonet, P., Jurkevitch, É., & Pasternak, Z. (2016) · Forensic Science International Genetics · doi:10.1016/j.fsigen.2016.10.005 · Cited by 50
The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci
Shukla, S. K., Ye, Z., Sandberg, S., Reyes, I., Fritsche, T. R., & Keifer, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183898 · Cited by 53
Molecular diversity of bacteria in commercially available “Spirulina” food supplements
Vardaka, E., Kormas, K. A., Katsiapi, M., Genitsaris, S., & Moustaka-Gouni, M. (2016) · PeerJ · doi:10.7717/peerj.1610 · Cited by 48
“Sequencing was performed as described in Dowd et al. (2008) in Roche 454 FLX titanium instruments and reagents after following manufacturer’s guidelines at the MRDNA Ltd. (Shallowater, TX, USA) sequencing facilities.”
Method
Bioprospecting of cowdung microflora for sustainable agricultural, biotechnological and environmental applications
Behera, S. S., & Ray, R. C. (2020) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2020.100018 · Cited by 50
“In most cases, fecal bacteia in cattle have been analyzed using culture-dependent methods that ave approximately 1% of the actual bacteria present in the animal gut Dowd et al., 2008 ; Wiegel et al., 2008 ; Vaishnav and Demain, 2009 ; allaway et al., 2010 ; Jami and Mizrahi, 2012 ).”
Method
Minor Changes in Soil Bacterial and Fungal Community Composition Occur in Response to Monsoon Precipitation in a Semiarid Grassland
McHugh, T. A., Koch, G. W., & Schwartz, E. (2014) · Microbial Ecology · doi:10.1007/s00248-014-0416-3 · Cited by 48
Intestinal Microbiota Succession and Immunomodulatory Consequences after Introduction of Lactobacillus reuteri I5007 in Neonatal Piglets
Hou, C., Liu, H. D., Zhang, J., Zhang, S., Yang, F., Zeng, X., Thacker, P. A., Zhang, G., & Qiao, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119505 · Cited by 49
“is a broad genus, and are ubiquitous in the gastrointestinal tract [40].”
Background
Characterization of a Drinking Water Distribution Pipeline Terminally Colonized byNaegleria fowleri
Morgan, M. J., Halstrom, S., Wylie, J. T., Walsh, T., Kaksonen, A. H., Sutton, D. C., Braun, K., & Puzon, G. J. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.5b05657 · Cited by 48
Dairy farm management practices and the risk of contamination of tank milk from Clostridium spp. and Paenibacillus spp. spores in silage, total mixed ration, dairy cow feces, and raw milk
Borreani, G., Ferrero, F., Nucera, D. M., Casale, M., Piano, S., & Tabacco, E. (2019) · Journal of Dairy Science · doi:10.3168/jds.2019-16462 · Cited by 48
“Therefore, new roles of clostridia in the intestinal tract may be speculated and would suggest their beneficial function in improving the digestion of complex OM, such as cellulose (Dowd et al., 2008).”
Background
Structure, dynamics and predicted functional role of the gut microbiota of the blue (Haliotis fulgens) and yellow (H. corrugata) abalone from Baja California Sur, Mexico
Cicala, F., Cisterna-Céliz, J. A., Moore, J. D., & Rocha‐Olivares, A. (2018) · PeerJ · doi:10.7717/peerj.5830 · Cited by 47
“Jd is a measure of dissimilarity for all pairwise combinations of a data set (Dowd et al., 2008) and was calculated using OTUs presence/absence.”
Method
Analysis of Black Fungal Biofilms Occurring at Domestic Water Taps (I): Compositional Analysis Using Tag-Encoded FLX Amplicon Pyrosequencing
Heinrichs, G., Hübner, I., Schmidt, C. K., de Hoog, S., & Haase, G. (2013) · Mycopathologia · doi:10.1007/s11046-013-9618-3 · Cited by 47
“analysis of the biofilms’ ribosomal internal transcribed spacer 2 (ITS2) region using Tag-Encoded FLX Amplicon Pyrosequencing (TEFAP), which has been used successfully in cases of bacterial communities recently [10].”
Method
Microbial profiles of liquid and solid fraction associated biomaterial in buffalo rumen fed green and dry roughage diets by tagged 16S rRNA gene pyrosequencing
Singh, K. M., Jisha, T. K., Reddy, B., Parmar, N. R., Patel, A., Patel, A., & Joshi, C. G. (2014) · Molecular Biology Reports · doi:10.1007/s11033-014-3746-9 · Cited by 47
Targeted 16S rRNA high-throughput sequencing to characterize microbial communities during composting of livestock mortalities
Tkachuk, V. L., Krause, D. O., Knox, N., Hamm, A. C., Zvomuya, F., Ominski, K., & McAllister, T. A. (2014) · Journal of Applied Microbiology · doi:10.1111/jam.12449 · Cited by 47
Microbial diversity and dynamics of a groundwater and a still bottled natural mineral water
França, L., López‐López, A., Rossello-Mora, R. A., & da Costa, M. S. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12430 · Cited by 47
Unraveling the Microbiota of Natural Black cv. Kalamata Fermented Olives through 16S and ITS Metataxonomic Analysis
Κάζου, Μ., Tzamourani, A. P., Panagou, E. Ζ., & Tsakalidou, E. (2020) · Microorganisms · doi:10.3390/microorganisms8050672 · Cited by 48
“Operational taxonomic units (OTUs) were defined after the removal of singleton sequences, clustered at 3% divergence (97% similarity) and taxonomically assigned using the Nucleotide Basic Local Alignment Search Tool (BLASTn) against a curated National Center for Biotechnology Information (NCBI) deriving database [34].”
Method
An in-depth analysis of actinobacterial communities shows their high diversity in grassland soils along a gradient of mixed heavy metal contamination
Větrovský, T., & Baldrián, P. (2015) · Biology and Fertility of Soils · doi:10.1007/s00374-015-1029-9 · Cited by 47
“Tag-encoded amplicon pyrosequencing of actinobacterial community The combination of a universal primer, eub530F (GTGCCA GCMGCNGCGG (Dowd et al. 2008)) and an Actinobacteriaspecific primer 16Sact1114r (GAGTTGACCCCGGCRGT, (Kyselkova et al. 2008)) was used to selectively amplify partial 16S sequences…”
BackgroundMethodInfluential
Butyryl/Caproyl-CoA:Acetate CoA-transferase: cloning, expression and characterization of the key enzyme involved in medium-chain fatty acid biosynthesis
Yang, Q., Guo, S., Lu, Q., Tao, Y., Zheng, D., Zhou, Q., & Liu, J. (2021) · Bioscience Reports · doi:10.1042/bsr20211135 · Cited by 46
Potential for using a hermetically-sealed, positive-pressured isocage system for studies involving germ-free mice outside a flexible-film isolator
Paik, J., Pershutkina, O. V., Meeker, S. M., Yi, J., Dowling, S. C., Hsu, C. C., Hajjar, A. M., Maggio‐Price, L., & Beck, D. A. C. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1064576 · Cited by 46
Bacterial community structure of a lab‐scale anammox membrane bioreactor
González‐Martínez, A., Osorio, F., Rodríguez–Sánchez, A., Martinez-Toledo, M. V., González-López, J., Lotti, T., & van Loosdrecht, M. C. M. (2014) · Biotechnology Progress · doi:10.1002/btpr.1995 · Cited by 46
Microbiological survey for analysis of the brown spots on the walls of the tomb of King Tutankhamun
Vasanthakumar, A., DeAraujo, A., Mazurek, J., Schilling, M. R., & Mitchell, R. (2013) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2013.01.014 · Cited by 46
In situ chemistry and microbial community compositions in five deep‐sea hydrothermal fluid samples from I rina II in the L ogatchev field
Perner, M., Gonnella, G., Hourdez, S., Böhnke, S., Kurtz, S., & Girguis, P. R. (2012) · Environmental Microbiology · doi:10.1111/1462-2920.12038 · Cited by 46
The role of bacterial communities and carbon dioxide on the corrosion of steel
Usher, K. M., Kaksonen, A. H., Bouquet, D., Cheng, K. Y., Geste, Y., Chapman, P., & Johnston, C. D. (2015) · Corrosion Science · doi:10.1016/j.corsci.2015.05.043 · Cited by 44
A snapshot of the microbiome of Amblyomma tuberculatum ticks infesting the gopher tortoise, an endangered species
Budachetri, K., Gaillard, D. L., Williams, J., Mukherjee, N., & Karim, S. (2016) · Ticks and Tick-borne Diseases · doi:10.1016/j.ttbdis.2016.07.010 · Cited by 46
Characterization of rumen, fecal, and milk microbiota in lactating dairy cows
Williamson, J., Callaway, T. R., Lourenco, J. M., & Ryman, V. E. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.984119 · Cited by 48
“Studying the microbiome allows us to understand which microbes live in or on animals, and the two most studied ecosystems in cattle are the ruminal and fecal microbiomes (Dowd et al., 2008).”
Background
Food-producing animals and their health in relation to human health
Téllez‐Isaías, G., Lauková, A., Latorre, J. D., Hernández-Velasco, X., Hargis, B. M., & Callaway, T. R. (2015) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v26.25876 · Cited by 46
“While much of our attention has been focused on the microbiome members that make up large proportions of the gastrointestinal population, members of other less known and/or less populous bacterial phyla have been isolated from gastrointestinal populations (82, 83).”
Background
Microbiome analysis and bacterial isolation from Lejía Lake soil in Atacama Desert
Mandaković, D., Maldonado, J. E., Pulgar, R., Cabrera, P., Gaete, A., Urtuvia, V., Seeger, M., Cambiazo, V., & González, M. (2018) · Extremophiles · doi:10.1007/s00792-018-1027-6 · Cited by 45
Effect of Acidic Industrial Effluent Release on Microbial Diversity and Trace Metal Dynamics During Resuspension of Coastal Sediment
Zouch, H., Cabrol, L., Chifflet, S., Tedetti, M., Karray, F., Zaghden, H., Sayadi, S., & Quéméneur, M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03103 · Cited by 48
“Bacterial and archaeal 16S rRNA genes were amplified by PCR using the 341F/815R prokaryotic universal primer set, as previously described by Dowd et al. (2008), and were sequenced by the MiSeq Illumina (paired-end 2 x 300 bp) platform of the Molecular Research Laboratory (Texas, USA).”
Method
Soil Bacterial Communities From the Chilean Andean Highlands: Taxonomic Composition and Culturability
Maza, F. R., Maldonado, J. E., Vásquez-Dean, J., Mandaković, D., Gaete, A., Cambiazo, V., & González, M. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00010 · Cited by 43
“Microbial 16S rRNA raw amplicon sequences were processed and analyzed following previously described protocols (Dowd et al., 2008; Handl et al., 2011).”
Method
Maturation of the Goat Rumen Microbiota Involves Three Stages of Microbial Colonization
Zhang, K., Li, B., Guo, M., Liu, G., Yang, Y., Wang, X., Chen, Y., & Zhang, E. (2019) · Animals · doi:10.3390/ani9121028 · Cited by 46
Impact of cigarette butts on microbial diversity and dissolved trace metals in coastal marine sediment
Quéméneur, M., Chifflet, S., Akrout, F., Zouari, A. B., & Hassen, M. B. (2020) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2020.106785 · Cited by 44
Shedding Light on the Microbial Community of the Macropod Foregut Using 454-Amplicon Pyrosequencing
Gulino, L.-M., Ouwerkerk, D., Kang, A. Y. H., Maguire, A. J., Kienzle, M., & Klieve, A. V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061463 · Cited by 44
Variations in 16S rRNA-based microbiome profiling between pyrosequencing runs and between pyrosequencing facilities
Kim, M., & Yu, Z. (2014) · The Journal of Microbiology · doi:10.1007/s12275-014-3443-3 · Cited by 44

Authors: Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., & Edrington, T. S.
Affiliations: Agricultural Research Service (US)
Corresponding author: Dowd, Scot E
ORCID: Dowd, Scot E
Callaway, Todd R
Edrington, Thomas S
Venue: BMC Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2008
Volume: 8
Issue: 1
Pages: 125
ISSN: 1471-2180 (ISSN-L)
DOI: 10.1186/1471-2180-8-125
PMC: PMC2515157
OpenAlex: W2105807803
Cited by: 1,121
References: 80
Citations by year: 2026: 16 · 2025: 23 · 2024: 32 · 2023: 32 · 2022: 45 · 2021: 65 · 2020: 52 · 2019: 60 · 2018: 68 · 2017: 105 · 2016: 116 · 2015: 121 · 2014: 129 · 2013: 99 · 2012: 75
FWCI: 11.37
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: BMC Microbiology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: U.S. Department of Agriculture
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Ruminant Nutrition and Digestive Physiology
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
Keywords: fecal microbiota, bacterial diversity, dairy cattle, Clostridium, Bacteroides, Ruminococcus, Lachnospiraceae, foodborne pathogens, Salmonella, Campylobacter, gut microbiota
MeSH terms: Animals, Bacteria, Cattle, DNA, Bacterial, DNA, Ribosomal, Feces, Female, RNA, Ribosomal, 16S, Polymerase Chain Reaction, Sequence Analysis, DNA, Gastrointestinal Tract, Biodiversity

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Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP)

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