Differences in ureolytic bacterial composition between the rumen digesta and rumen wall based on ureC gene classification

Jin, D.; Zhao, S.; Zheng, N.; Bu, D.; Beckers, Yves; Denman, S. E.; McSweeney, C. S.; Wang, J.

doi:10.3389/fmicb.2017.00385

Article (Scientific journals)

Differences in ureolytic bacterial composition between the rumen digesta and rumen wall based on ureC gene classification

Jin, D.; Zhao, S.; Zheng, N. et al.

2017 • In Frontiers in Microbiology, 8 (MAR)

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/221048

DOI
10.3389/fmicb.2017.00385

PubMed
28326079

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

FIM_2017_Jin.pdf

Publisher postprint (2.09 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Difference; Rumen digesta; Rumen wall; UreC gene; Ureolytic bacteria; Article; Clostridiaceae; Helicobacteraceae; Marinobacter; Methylococcaceae; Methylophilaceae; Oxalobacteraceae; Paenibacillaceae

Abstract :

[en] Ureolytic bacteria are key organisms in the rumen producing urease enzymes to catalyze the breakdown of urea to ammonia for the synthesis of microbial protein. However, little is known about the diversity and distribution of rumen ureolytic microorganisms. The urease gene (ureC) has been the target gene of choice for analysis of the urea-degrading microorganisms in various environments. In this study, we investigated the predominant ureC genes of the ureolytic bacteria in the rumen of dairy cows using high-throughput sequencing. Six dairy cows with rumen fistulas were assigned to a two-period cross-over trial. A control group (n = 3) were fed a total mixed ration without urea and the treatment group (n = 3) were fed rations plus 180 g urea per cow per day at three separate times. Rumen bacterial samples from liquid and solid digesta and rumen wall fractions were collected for ureC gene amplification and sequencing using Miseq. The wall-adherent bacteria (WAB) had a distinct ureolytic bacterial profile compared to the solid-adherent bacteria (SAB) and liquid-associated bacteria (LAB) but more than 55% of the ureC sequences did not affiliate with any known taxonomically assigned urease genes. Diversity analysis of the ureC genes showed that the Shannon and Chao1 indices for the rumen WAB was lower than those observed for the SAB and LAB (P < 0.01). The most abundant ureC genes were affiliated with Methylococcaceae, Clostridiaceae, Paenibacillaceae, Helicobacteraceae, and Methylophilaceae families. Compared with the rumen LAB and SAB, relative abundance of the OTUs affiliated with Methylophilus and Marinobacter genera were significantly higher (P < 0.05) in the WAB. Supplementation with urea did not alter the composition of the detected ureolytic bacteria. This study has identified significant populations of ureolytic WAB representing genera that have not been recognized or studied previously in the rumen. The taxonomic classification of rumen ureC genes in the dairy cow indicates that the majority of ureolytic bacteria are yet to be identified. This survey has expanded our knowledge of ureC gene information relating to the rumen ureolytic microbial community, and provides a basis for obtaining regulatory targets of ureolytic bacteria to moderate urea hydrolysis in the rumen. © 2017 Jin, Zhao, Zheng, Bu, Beckers, Denman, McSweeney and Wang.

Disciplines :

Animal production & animal husbandry

Author, co-author :

Jin, D.; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, Precision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium, Lab. of Quality and Safety Risk Assessment for Dairy Products of Ministry of Agriculture (Beijing), Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Zhao, S.; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, Lab. of Quality and Safety Risk Assessment for Dairy Products of Ministry of Agriculture (Beijing), Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Zheng, N.; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, Lab. of Quality and Safety Risk Assessment for Dairy Products of Ministry of Agriculture (Beijing), Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Bu, D.; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Beckers, Yves ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition

Denman, S. E.; Commonwealth Scientific and Industrial Research Organisation, Queensland Bioscience Precinct, St. Lucia, QLD, Australia

McSweeney, C. S.; Commonwealth Scientific and Industrial Research Organisation, Queensland Bioscience Precinct, St. Lucia, QLD, Australia

Wang, J.; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, Lab. of Quality and Safety Risk Assessment for Dairy Products of Ministry of Agriculture (Beijing), Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Language :

English

Title :

Differences in ureolytic bacterial composition between the rumen digesta and rumen wall based on ureC gene classification

Publication date :

2017

Journal title :

Frontiers in Microbiology

eISSN :

1664-302X

Publisher :

Frontiers Research Foundation

Volume :

Issue :

MAR

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 March 2018

Statistics

Number of views

63 (2 by ULiège)

Number of downloads

107 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Agle, M., Hristov, A. N., Zaman, S., Schneider, C., Ndegwa, P., and Vaddella, V. K. (2010). The effects of ruminally degraded protein on rumen fermentation and ammonia losses from manure in dairy cows. J. Dairy Sci. 93, 1625-1637. doi: 10.3168/jds.2009-2579
Albertsen, M., Karst, S. M., Ziegler, A. S., Kirkegaard, R. H., and Nielsen, P. H. (2015). Back to basics-the influence of DNA extraction and primer choice on phylogenetic analysis of activated sludge communities. PLoS ONE 10:e0132783. doi: 10.1371/journal.pone.0132783
Boden, R., Cunliffe, M., Scanlan, J., Moussard, H., Kits, K. D., Klotz, M. G., et al. (2011). Complete genome sequence of the aerobic marine methanotroph Methylomonas methanica MC09. J. Bacteriol. 193, 7001-7002. doi: 10.1128/JB.06267-11
Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., et al. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Meth. 10, 57-59. doi: 10.1038/nmeth.2276
Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. doi: 10.1093/bioinformatics/btu170
Broderick, G. A., and Kang, J. H. (1980). Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. J. Dairy Sci. 63, 64-75. doi: 10.3168/jds.S0022-0302(80)82888-8
Burbank, M. B., Weaver, T. J., Williams, B. C., and Crawford, R. L. (2012). Urease activity of ureolytic bacteria isolated from six soils in which calcite was precipitated by indigenous bacteria. Geomicrobiol. J. 29, 389-395. doi: 10.1080/01490451.2011.575913
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., and Bushman, F. D. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 336-336. doi: 10.1038/nmeth0510-335
Carter, E. L., Flugga, N., Boer, J. L., Mulrooney, S. B., and Hausinger, R. P. (2009). Interplay of metal ions and urease. Metallomics 1, 207-221. doi: 10.1039/b903311d
Ceconi, I., Ruiz-Moreno, M. J., DiLorenzo, N., DiCostanzo, A., and Crawford, G. I. (2015). Effect of urea inclusion in diets containing corn dried distillers grains on feedlot cattle performance, carcass characteristics, ruminal fermentation, total tract digestibility, and purine derivatives-to-creatinine index. J. Anim. Sci. 93, 357-369. doi: 10.2527/jas.2014-8214
Chessel, D., Dufour, A. B., and Thioulouse, J. (2004). The ade4 package-I-one-table methods. R News 4, 5-10
Coldham, T., Rose, K., O'Rourke, J., Neilan, B. A., Dalton, H., Lee, A., et al. (2011). Detection, isolation, and characterization of Helicobacter species from the gastrointestinal tract of the brushtail possum. Appl. Environ. Microbiol. 77, 1581-1587. doi: 10.1128/AEM.01960-10
Collier, J. L., Baker, K. M., and Bell, S. L. (2009). Diversity of urea-degrading microorganisms in open-ocean and estuarine planktonic communities. Environ. Microbiol. 11, 3118-3131. doi: 10.1111/j.1462-2920.2009.02016.x
Collins, C. M., and D'Orazio, S. E. (1993). Bacterial ureases: structure, regulation of expression and role in pathogenesis. Mol. Microbiol. 9, 907-913. doi: 10.1111/j.1365-2958.1993.tb01220.x
Cook, A. (1976). Urease activity in the rumen of sheep and the isolation of ureolytic bacteria. J. Gen. Microbiol. 92, 32-48. doi: 10.1099/00221287-92-1-32
Cook, A. R., Riley, P. W., Murdoch, H., Evans, P. N., and McDonald, I. R. (2007). Howardella ureilytica gen. nov., sp. nov., a Gram-positive, coccoid-shaped bacterium from a sheep rumen. Int. J. Syst. Evol. Microbiol. 57, 2940-2945. doi: 10.1099/ijs.0.64819-0
Dianou, D., and Adachi, K. (1999). Characterization of methanotrophic bacteria isolated from a subtropical paddy field. FEMS Microbiol. Lett. 173, 163-173. doi: 10.1111/j.1574-6968.1999.tb13498.x
Doronina, N., Ivanova, E., Trotsenko, Y., Pshenichnikova, A., Kalinina, E., and Shvets, V. (2005). Methylophilus quaylei sp. nov., a new aerobic obligately methylotrophic bacterium. Syst. Appl. Microbiol. 28, 303-309. doi: 10.1016/j.syapm.2005.02.002
Duran, R. (2010). "Marinobacter," in Handbook of Hydrocarbon and Lipid Microbiology, ed. K. N. Timmis (Berlin: Springer-Verlag), 1725-1735
Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
Edwards, J. E., McEwan, N. R., Travis, A. J., and Wallace, R. J. (2004). 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie Van Leeuwenhoek 86, 263-281. doi: 10.1023/B:ANTO.0000047942.69033.24
Fox, J. (2002). The non-H pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50, 273-283. doi: 10.1136/gut.50.2.273
Gaujoux, R., and Seoighe, C. (2010). A flexible R package for nonnegative matrix factorization. BMC Bioinformatics 11:367. doi: 10.1186/1471-2105-11-367
Greenwood, J. A., Mills, J., Tyler, P. D., and Jones, C. W. (1998). Physiological regulation, purification and properties of urease from Methylophilus methylotrophus. FEMS Microbiol. Lett. 160, 131-135. doi: 10.1111/j.1574-6968.1998.tb12902.x
Harper, C. G., Feng, Y., Xu, S., Taylor, N. S., Kinsel, M., Dewhirst, F. E., et al. (2002). Helicobacter cetorum sp. nov., a urease-positive Helicobacter species isolated from dolphins and whales. J. Clin. Microbiol. 40, 4536-4543. doi: 10.1128/jcm.40.12.4536-4543.2002
Harper, C. G., Whary, M. T., Feng, Y., Rhinehart, H. L., Wells, R. S., Xu, S., et al. (2003). Comparison of diagnostic techniques for Helicobacter cetorum infection in wild Atlantic bottlenose dolphins (Tursiops truncatus). J. Clin. Microbiol. 41, 2842-2848. doi: 10.1128/JCM.41.7.2842-2848.2003
Hoefman, S., Heylen, K., and De Vos, P. (2014). Methylomonas lenta sp. nov., a methanotroph isolated from manure and a denitrification tank. Int. J. Syst. Evol. Microbiol. 64, 1210-1217. doi: 10.1099/ijs.0.057794-0
Kakimoto, S., Okazaki, K., Sakane, T., Imai, K., Sumino, Y., Akiyama, S.-I., et al. (1989). Isolation and taxonomie characterization of acid urease-producing bacteria. Agric. Biol. Chem. 53, 1111-1117. doi: 10.1080/00021369.1989.10869439
Kertz, A. F. (2010). Review: urea feeding to dairy cattle: a historical perspective and review. Prof. Anim. Sci. 26, 257-272. doi: 10.15232/S1080-7446(15)30593-3
Lauková, A., and Koniarová, I. (1994). Survey of urease activity in ruminal bacteria isolated from domestic and wild ruminants. Microbios 84, 7-11
Lebzien, P. (2006). Nitrogen and phosphorus nutrition of cattle. Anim. Feed Sci. Tech. 128, 342-343. doi: 10.1016/j.anifeedsci.2006.01.027
Love, M. I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550. doi: 10.1186/s13059-014-0550-8
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Buchner, A., et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi: 10.1093/nar/gkh293
Madhaiyan, M., Poonguzhali, S., Kwon, S. W., and Sa, T. M. (2009). Methylophilus rhizosphaerae sp. nov., a restricted facultative methylotroph isolated from rice rhizosphere soil. Int. J. Syst. Evol. Microbiol. 59, 2904-2908. doi: 10.1099/ijs.0.009811-0
Magoè, T., and Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963. doi: 10.1093/bioinformatics/btr507
Matsen, F. A., Kodner, R. B., and Armbrust, E. V. (2010). pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11:538. doi: 10.1186/1471-2105-11-538
McMurdie, P. J., and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. doi: 10.1371/journal.pone.0061217
Mills, J., Wyborn, N. R., Greenwood, J. A., Williams, S. G., and Jones, C. W. (1998). Characterisation of a binding-protein-dependent, active transport system for short-chain amides and urea in the methylotrophic bacterium Methylophilus methylotrophus. Eur. J. Biochem. 251, 45-53. doi: 10.1046/j.1432-1327.1998.2510045.x
Milton, C., Brandt, R. Jr., and Titgemeyer, E. (1997). Urea in dry-rolled corn diets: finishing steer performance, nutrient digestion, and microbial protein production. J. Anim. Sci. 75, 1415-1424. doi: 10.2527/1997.7551415x
Minas, K., McEwan, N. R., Newbold, C. J., and Scott, K. P. (2011). Optimization of a high-throughput CTAB-based protocol for the extraction of qPCR-grade DNA from rumen fluid, plant and bacterial pure cultures. FEMS Microbiol. Lett. 325, 162-169. doi: 10.1111/j.1574-6968.2011.02424.x
Mobley, H., Island, M. D., and Hausinger, R. P. (1995). Molecular biology of microbial ureases. Microbiol. Rev. 59, 451-480
On, S., Atabay, H., Corry, J., Harrington, C., and Vandamme, P. (1998). Emended description of Campylobacter sputorum and revision of its infrasubspecific (biovar) divisions, including C. sputorum biovar paraureolyticus, a urease-producing variant from cattle and humans. Int. J. Syst. Bacteriol. 48, 195-206. doi: 10.1099/00207713-48-1-195
Owens, F. N., Lusby, K. S., Mizwicki, K., and Forero, O. (1980). Slow ammonia release from urea: rumen and metabolism studies. J. Anim. Sci. 50, 527-531. doi: 10.2527/jas1980.503527x
Patra, A. K. (2015). "Urea/ammonia metabolism in the rumen and toxicity in ruminants," in Rumen Microbiology: From Evolution to Revolution, eds A. K. Puniya, R. Singh, and D. N. Kamra (New Delhi: Springer), 329-341
Petri, R., Schwaiger, T., Penner, G., Beauchemin, K., Forster, R., McKinnon, J., et al. (2013). Changes in the rumen epimural bacterial diversity of beef cattle as affected by diet and induced ruminal acidosis. Appl. Environ. Microbiol. 79, 3744-3755. doi: 10.1128/AEM.03983-12
Price, M. N., Dehal, P. S., and Arkin, A. P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650. doi: 10.1093/molbev/msp077
Recktenwald, E. B., Ross, D. A., Fessenden, S. W., Wall, C. J., and Van Amburgh, M. E. (2014). Urea-N recycling in lactating dairy cows fed diets with 2 different levels of dietary crude protein and starch with or without monensin. J. Dairy Sci. 97, 1611-1622. doi: 10.3168/jds.2013-7162
Reed, K. E. (2001). Restriction enzyme mapping of bacterial urease genes: using degenerate primers to expand experimental outcomes. Biochem. Mol. Biol. Educ. 29, 239-244. doi: 10.1111/j.1539-3429.2001.tb00131.x
Singer, E., Webb, E. A., Nelson, W. C., Heidelberg, J. F., Ivanova, N., Pati, A., et al. (2011). Genomic potential of Marinobacter aquaeolei, a biogeochemical "opportunitroph". Appl. Environ. Microbiol. 77, 2763-2771. doi: 10.1128/AEM.01866-10
Singh, B. K., Nunan, N., and Millard, P. (2009). Response of fungal, bacterial and ureolytic communities to synthetic sheep urine deposition in a grassland soil. FEMS Microbiol. Ecol. 70, 109-117. doi: 10.1111/j.1574-6941.2009.00731.x
Sonnhammer, E. L., and Hollich, V. (2005). Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinformatics 6:108. doi: 10.1186/1471-2105-6-108
Soren, N., Malik, P., Sejian, V., Bhatta, R., Takahashi, J., Kohn, R., et al. (2015). "Methanotrophs in enteric methane mitigation," in Livestock Production and Climate Change, eds P. K. Malik, R. Bhatta, J. Takaha-shi, R. A. Kohn, and C. S. Prasad (Boston, MA: CABI), 360
Su, J., Jin, L., Jiang, Q., Sun, W., Zhang, F., and Li, Z. (2013). Phylogenetically diverse ureC genes and their expression suggest the urea utilization by bacterial symbionts in marine sponge Xestospongia testudinaria. PLoS ONE 8:e64848. doi: 10.1371/journal.pone.0064848
Wagner, J. J., Engle, T. E., and Bryant, T. C. (2010). The effect of rumen degradable and rumen undegradable intake protein on feedlot performance and carcass merit in heavy yearling steers. J. Anim. Sci. 88, 1073-1081. doi: 10.2527/jas.2009-2111
Weeks, D. L., and Sachs, G. (2001). Sites of pH regulation of the urea channel of Helicobacter pylori. Mol. Microbiol. 40, 1249-1259. doi: 10.1046/j.1365-2958.2001.02466.x
Wozny, M., Bryant, M., Holdeman, L. T., and Moore, W. (1977). Urease assay and urease-producing species of anaerobes in the bovine rumen and human feces. Appl. Environ. Microbiol. 33, 1097-1104
Zhao, S., Wang, J., Zheng, N., Bu, D., Sun, P., and Yu, Z. (2015). Reducing microbial ureolytic activity in the rumen by immunization against urease therein. BMC Vet. Res. 11:94. doi: 10.1186/s12917-015-0409-6
Zotta, T., Ricciardi, A., Rossano, R., and Parente, E. (2008). Urease production by Streptococcus thermophilus. Food Microbiol. 25, 113-119. doi: 10.1016/j.fm.2007.07.001