Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep

Kamke, Janine; Soni, Priya; Li, Yang; Ganesh, Siva; Kelly, William J.; Leahy, Sinead C.; Shi, Weibing; Froula, Jeff; Rubin, Edward M.; Attwood, Graeme T.

doi:10.1186/s13104-017-2671-0

Title: Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep

Journal Article · Tue Aug 08 00:00:00 EDT 2017 · BMC Research Notes

DOI:https://doi.org/10.1186/s13104-017-2671-0· OSTI ID:1629215

Kamke, Janine ^[1]; Soni, Priya ^[1]; Li, Yang ^[1]; Ganesh, Siva ^[1]; Kelly, William J. ^[1]; Leahy, Sinead C. ^[1]; Shi, Weibing ^[2]; Froula, Jeff ^[2]; Rubin, Edward M. ^[2];

^[1]

AgResearch Limited, Palmerston (New Zealand). Grasslands Research Centre
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division

Background: Ruminants are important contributors to global methane emissions via microbial fermentation in their reticulo-rumens. This study is part of a larger program, characterising the rumen microbiomes of sheep which vary naturally in methane yield (g CH4/kg DM/day) and aims to defne diferences in microbial communities, and in gene and transcript abundances that can explain the animal methane phenotype. Methods: Rumen microbiome metagenomic and metatranscriptomic data were analysed by Gene Set Enrichment, sparse partial least squares regression and the Wilcoxon Rank Sum test to estimate correlations between specifc KEGG bacterial pathways/genes and high methane yield in sheep. KEGG genes enriched in high methane yield sheep were reassembled from raw reads and existing contigs and analysed by MEGAN to predict their phylogenetic origin. Protein coding sequences from Succinivibrio dextrinosolvens strains were analysed using Efective DB to predict bacterial type III secreted proteins. The efect of S. dextrinosolvens strain H5 growth on methane formation by rumen methanogens was explored using co-cultures. Results: Detailed analysis of the rumen microbiomes of high methane yield sheep shows that gene and transcript abundances of bacterial type III secretion system genes are positively correlated with methane yield in sheep. Most of the bacterial type III secretion system genes could not be assigned to a particular bacterial group, but several genes were afliated with the genus Succinivibrio, and searches of bacterial genome sequences found that strains of S. dextrinosolvens were part of a small group of rumen bacteria that encode this type of secretion system. In co-culture experiments, S. dextrinosolvens strain H5 showed a growth-enhancing efect on a methanogen belonging to the order Methanomassiliicoccales, and inhibition of a representative of the Methanobrevibacter gottschalkii clade. Conclusions: This is the frst report of bacterial type III secretion system genes being associated with high methane emissions in ruminants, and identifes these secretions systems as potential new targets for methane mitigation research. The effects of S. dextrinosolvens on the growth of rumen methanogens in co-cultures indicate that bacteriamethanogen interactions are important modulators of methane production in ruminant animals.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1629215

Journal Information:: BMC Research Notes, Vol. 10, Issue 1; ISSN 1756-0500

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores Pope, P. B.; Denman, S. E.; Jones, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1005297107	journal	July 2010
IMG/M 4 version of the integrated metagenome comparative analysis system Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573 https://doi.org/10.1093/nar/gkt919	journal	October 2013
High-Yield and Phylogenetically Robust Methods of DNA Recovery for Analysis of Microbial Biofilms Adherent to Plant Biomass in the Herbivore Gut Rosewarne, Carly P.; Pope, Phillip B.; Denman, Stuart E. Microbial Ecology, Vol. 61, Issue 2 https://doi.org/10.1007/s00248-010-9745-z	journal	September 2010
Rumen function and digestion parameters associated with differences between sheep in methane emissions when fed chaffed lucerne hay Pinares-PatiÑO, C. S.; Ulyatt, M. J.; Lassey, K. R. The Journal of Agricultural Science, Vol. 140, Issue 2 https://doi.org/10.1017/s0021859603003046	journal	March 2003
Illumina MiSeq Phylogenetic Amplicon Sequencing Shows a Large Reduction of an Uncharacterised Succinivibrionaceae and an Increase of the Methanobrevibacter gottschalkii Clade in Feed Restricted Cattle McCabe, Matthew Sean; Cormican, Paul; Keogh, Kate PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0133234	journal	July 2015
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Simultaneous Amplicon Sequencing to Explore Co-Occurrence Patterns of Bacterial, Archaeal and Eukaryotic Microorganisms in Rumen Microbial Communities Kittelmann, Sandra; Seedorf, Henning; Walters, William A. PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0047879	journal	February 2013
Horizontal gene transfer enables programmable gene stability in synthetic microbiota Wang, Teng; Weiss, Andrea; Aqeel, Ammara Nature Chemical Biology, Vol. 18, Issue 11 https://doi.org/10.1038/s41589-022-01114-3	journal	September 2022
Is rumen retention time implicated in sheep differences in methane emission? Pinares-Patiño, C. S.; Ebrahimi, S. H.; Mcewan, J. C. Unpublished https://doi.org/10.13140/2.1.3309.5043	text	January 2011
Retention time of digesta in the rumen: its repeatability and relationship with wool production of Merino rams. Smuts, M.; Meissner, H. H.; Cronjé, P. B. Journal of Animal Science, Vol. 73, Issue 1 https://doi.org/10.2527/1995.731206x	journal	January 1995
Normal Flora—Rumen Bacteria Bryant, M. P. The American Journal of Clinical Nutrition, Vol. 23, Issue 11 https://doi.org/10.1093/ajcn/23.11.1440	journal	November 1970
Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium Kenters, Nikki; Henderson, Gemma; Jeyanathan, Jeyamalar Journal of Microbiological Methods, Vol. 84, Issue 1 https://doi.org/10.1016/j.mimet.2010.10.011	journal	January 2011
Bacterial Type III Secretion Systems: Specialized Nanomachines for Protein Delivery into Target Cells Galán, Jorge E.; Lara-Tejero, Maria; Marlovits, Thomas C. Annual Review of Microbiology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-micro-092412-155725	journal	September 2014
Characteristics of two new Genera of Anaerobic Curved rods Isolated from the Rumen of Cattle Bryant, Marvin P.; Small, Nola Journal of Bacteriology, Vol. 72, Issue 1 https://doi.org/10.1128/jb.72.1.22-26.1956	journal	January 1956
Functional domains and motifs of bacterial type III effector proteins and their roles in infection Dean, Paul FEMS Microbiology Reviews, Vol. 35, Issue 6 https://doi.org/10.1111/j.1574-6976.2011.00271.x	journal	November 2011
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Trojan Horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment Barker, J.; Brown, M. R. W. Microbiology, Vol. 140, Issue 6 https://doi.org/10.1099/00221287-140-6-1253	journal	June 1994
Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation Kamke, Janine; Kittelmann, Sandra; Soni, Priya Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0201-2	journal	October 2016
Genetic parameters for predicted methane production and laser methane detector measurements1 Pickering, N. K.; Chagunda, M. G. G.; Banos, G. Journal of Animal Science, Vol. 93, Issue 1 https://doi.org/10.2527/jas.2014-8302	journal	January 2015
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Bacteroides Ruminicola n. sp. and Succinimonas Amylolytica the new Genus and Species Bryant, M. P.; Small, Nola; Bouma, Cecelia Journal of Bacteriology, Vol. 76, Issue 1 https://doi.org/10.1128/JB.76.1.15-23.1958	journal	January 1958
Changes in the Rumen Epimural Bacterial Diversity of Beef Cattle as Affected by Diet and Induced Ruminal Acidosis Petri, R. M.; Schwaiger, T.; Penner, G. B. Applied and Environmental Microbiology, Vol. 79, Issue 12 https://doi.org/10.1128/AEM.03983-12	journal	April 2013
Bacteremia Due to Succinivibrio dextrinosolvens : Report of a Case Southern, Paul M. American Journal of Clinical Pathology, Vol. 64, Issue 4 https://doi.org/10.1093/ajcp/64.4.540	journal	October 1975
Classification of the spore-forming sulfate-reducing bacteria Campbell, L. L.; Postgate, J. R. Bacteriological Reviews, Vol. 29, Issue 3 https://doi.org/10.1128/br.29.3.359-363.1965	journal	September 1965
Microbiota-accessible carbohydrates suppress Clostridium difficile infection in a murine model Hryckowian, Andrew J.; Van Treuren, William; Smits, Samuel A. Nature Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/s41564-018-0150-6	journal	April 2018
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Repeatability of methane emissions from sheep Pinares-Patiño, C. S.; McEwan, J. C.; Dodds, K. G. Animal Feed Science and Technology, Vol. 166-167 https://doi.org/10.1016/j.anifeedsci.2011.04.068	journal	June 2011
Integrative analysis of environmental sequences using MEGAN4 Huson, D. H.; Mitra, S.; Ruscheweyh, H. -J. Genome Research, Vol. 21, Issue 9 https://doi.org/10.1101/gr.120618.111	journal	June 2011
Rhizobial secreted proteins as determinants of host specificity in the rhizobiumâlegume symbiosis Fauvart, Maarten; Michiels, Jan FEMS Microbiology Letters, Vol. 285, Issue 1 https://doi.org/10.1111/j.1574-6968.2008.01254.x	journal	August 2008
Isolation and Presumptive Identification of Adherent Epithelial Bacteria (“Epimural” Bacteria) from the Ovine Rumen Wall Mead, Lorna J.; Jones, G. A. Applied and Environmental Microbiology, Vol. 41, Issue 4 https://doi.org/10.1128/AEM.41.4.1020-1028.1981	journal	January 1981
Rumen Differences between Sheep Identified as being Low or High Methane Emitters Bain¹, W. E.; Bezuidenhout¹, L.; Jopson², N. B. Unpublished https://doi.org/10.13140/2.1.3702.7206	text	January 2014
Ab initio gene identification in metagenomic sequences Zhu, Wenhan; Lomsadze, Alexandre; Borodovsky, Mark Nucleic Acids Research, Vol. 38, Issue 12 https://doi.org/10.1093/nar/gkq275	journal	April 2010
Methane emission by sectors: A comprehensive review of emission sources and mitigation methods Yusuf, Rafiu O.; Noor, Zainura Z.; Abba, Ahmad H. Renewable and Sustainable Energy Reviews, Vol. 16, Issue 7 https://doi.org/10.1016/j.rser.2012.04.008	journal	September 2012
Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range Henderson, Gemma; Cox, Faith; Ganesh, Siva Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14567	journal	October 2015
Improved extraction of PCR-quality community DNA from digesta and fecal samples Yu, Zhongtang; Morrison, Mark BioTechniques, Vol. 36, Issue 5 https://doi.org/10.2144/04365ST04	journal	May 2004
Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range Henderson, Gemma; Cox, Faith; Ganesh, Siva ETH Zurich https://doi.org/10.3929/ethz-b-000164426	text	January 2015
gp130/STAT3 signaling is required for homeostatic proliferation and anabolism in postnatal growth plate and articular chondrocytes Liu, Nancy Q.; Lin, Yucheng; Li, Liangliang Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-021-02944-y	journal	January 2022
GSEA-P: a desktop application for Gene Set Enrichment Analysis Subramanian, Aravind; Kuehn, Heidi; Gould, Joshua Bioinformatics, Vol. 23, Issue 23 https://doi.org/10.1093/bioinformatics/btm369	journal	July 2007
“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens Paul, Kristina; Nonoh, James O.; Mikulski, Lena Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/AEM.02193-12	journal	September 2012
Physiological Ecology of Methanogens Zinder, Stephen H. Methanogenesis https://doi.org/10.1007/978-1-4615-2391-8_4	book	January 1993
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Genetic and environmental variation in methane emissions of sheep at pasture1 Robinson, D. L.; Goopy, J. P.; Hegarty, R. S. Journal of Animal Science, Vol. 92, Issue 10 https://doi.org/10.2527/jas.2014-8042	journal	October 2014
Anaerobic vibrio-like organisms cultured from blood: Desulfovibrio desulfuricans and Succinivibrio species Porschen, R. K.; Chan, P. Journal of Clinical Microbiology, Vol. 5, Issue 4 https://doi.org/10.1128/jcm.5.4.444-447.1977	journal	April 1977
Effect of Methanobrevibacter smithii on Xylanolytic Activity of Anaerobic Ruminal Fungi Joblin, K. N.; Naylor, G. E.; Williams, A. G. Applied and Environmental Microbiology, Vol. 56, Issue 8 https://doi.org/10.1128/aem.56.8.2287-2295.1990	journal	January 1990
Description of Methanobrevibacter gottschalkii sp. nov., Methanobrevibacter thaueri sp. nov., Methanobrevibacter woesei sp. nov. and Methanobrevibacter wolinii sp. nov.. Miller, Terry L.; Lin, Chuzhao International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 3 https://doi.org/10.1099/00207713-52-3-819	journal	May 2002
Methane emissions measured directly from grazing livestock in New Zealand Lassey, Keith R.; Ulyatt, Marcus J.; Martin, Ross J. Atmospheric Environment, Vol. 31, Issue 18 https://doi.org/10.1016/s1352-2310(97)00123-4	journal	September 1997
Bacterial Species of the Rumen Bryant, Marvin P. Bacteriological Reviews, Vol. 23, Issue 3 https://doi.org/10.1128/br.23.3.125-153.1959	journal	September 1959
The rumen microbial metagenome associated with high methane production in cattle Wallace, R. John; Rooke, John A.; McKain, Nest BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2032-0	journal	October 2015
Methanogens: Methane Producers of the Rumen and Mitigation Strategies Hook, Sarah E.; Wright, André-Denis G.; McBride, Brian W. Archaea, Vol. 2010 https://doi.org/10.1155/2010/945785	journal	January 2010
A study on consistency of differences between cows in rumen outflow rate of fibrous particles and other substrates and consequences for digestibility and intake of roughages Ørskov, E. R.; Ojwang, I.; Reid, G. W. Animal Science, Vol. 47, Issue 1 https://doi.org/10.1017/S000335610003703X	journal	August 1988
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Classification of the spore-forming sulfate-reducing bacteria. Campbell, L. L.; Postgate, J. R. Bacteriological Reviews, Vol. 29, Issue 3 https://doi.org/10.1128/MMBR.29.3.359-363.1965	journal	January 1965
Low-methane yield sheep have smaller rumens and shorter rumen retention time Goopy, John P.; Donaldson, Alastair; Hegarty, Roger British Journal of Nutrition, Vol. 111, Issue 4 https://doi.org/10.1017/S0007114513002936	journal	October 2013
Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome Shi, Weibing; Moon, Christina D.; Leahy, Sinead C. Genome Research, Vol. 24, Issue 9 https://doi.org/10.1101/gr.168245.113	journal	June 2014
Heritability estimates of methane emissions from sheep Pinares-Patiño, C. S.; Hickey, S. M.; Young, E. A. animal, Vol. 7, Issue s2 https://doi.org/10.1017/s1751731113000864	journal	June 2013
Evaluation of dietary strategies to reduce methane production in ruminants: A modelling approach Benchaar, C.; Pomar, C.; Chiquette, J. Canadian Journal of Animal Science, Vol. 81, Issue 4 https://doi.org/10.4141/a00-119	journal	December 2001
EffectiveDB—updates and novel features for a better annotation of bacterial secreted proteins and Type III, IV, VI secretion systems Eichinger, Valerie; Nussbaumer, Thomas; Platzer, Alexander Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1269	journal	November 2015
Bacterial Species of the Rumen Bryant, Marvin P. Bacteriological Reviews, Vol. 23, Issue 3 https://doi.org/10.1128/MMBR.23.3.125-153.1959	journal	January 1959
Sire and liveweight affect feed intake and methane emissions of sheep confined in respiration chambers Robinson, D. L.; Goopy, J. P.; Donaldson, A. J. Animal, Vol. 8, Issue 12 https://doi.org/10.1017/s1751731114001773	journal	January 2014
Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes Vangelisti, Alberto; Guidi, Lucia; Cavallini, Andrea Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58878-8	journal	February 2020
Fermentation of methanol in the sheep rumen. Pol, A.; Demeyer, D. I. Applied and Environmental Microbiology, Vol. 54, Issue 3 https://doi.org/10.1128/aem.54.3.832-834.1988	journal	January 1988
Measures of methane production and their phenotypic relationships with dry matter intake, growth, and body composition traits in beef cattle1,2 Herd, R. M.; Arthur, P. F.; Donoghue, K. A. Journal of Animal Science, Vol. 92, Issue 11 https://doi.org/10.2527/jas.2014-8273	journal	November 2014

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59 BASIC BIOLOGICAL SCIENCES
Rumen
Methane
Bacterial
Type III secretion
Succinivibrio

MOESM1 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/m9.figshare.c.3846796_d1.v1 The current record is supplemented by this dataset	dataset	January 2017
Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/m9.figshare.c.3846796.v1 The current record is supplemented by this collection	collection	January 2017
Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/m9.figshare.c.3846796 The current record is supplemented by this collection	collection	January 2017
MOESM3 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/m9.figshare.c.3846796_d3.v1 The current record is supplemented by this dataset	dataset	January 2017
MOESM2 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/m9.figshare.c.3846796_d2.v1 The current record is supplemented by this dataset	dataset	January 2017
MOESM2 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/M9.FIGSHARE.C.3846796_D2 The current record is supplemented by this dataset	dataset	January 2017
MOESM3 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/M9.FIGSHARE.C.3846796_D3 The current record is supplemented by this dataset	dataset	January 2017
MOESM1 of Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep Kamke, Janine; Soni, Priya; Li, Yang https://doi.org/10.6084/M9.FIGSHARE.C.3846796_D1 The current record is supplemented by this dataset	dataset	January 2017

Title: Gene and transcript abundances of bacterial type III secretion systems from the rumen microbiome are correlated with methane yield in sheep

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