Rumen protozoa and methanogenesis: not a simple cause–effect relationship
Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep ha...
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Published in: | British journal of nutrition Vol. 107; no. 3; pp. 388 - 397 |
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Main Authors: | , , , |
Format: | Journal Article |
Language: | English |
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Cambridge, UK
Cambridge University Press
14-02-2012
Cambridge University Press (CUP) |
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Abstract | Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D − ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D − and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D − were the lowest ( − 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D − animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. |
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AbstractList | Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D − ) or for more than 2 years (D+)) were used in
in vitro
and
in vivo
experiments.
In vitro
the absence of protozoa decreased NH
3
and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D − and F inoculum (
P
< 0·05).
In vivo
fermentation parameters of donor animals showed the same trend on NH
3
and butyrate and showed that D+ animals were high methane emitters, while D − were the lowest ( − 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D − animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D - ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D - and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D - were the lowest ( - 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D - animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. [PUBLICATION ABSTRACT] Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D − ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D − and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D − were the lowest ( − 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D − animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D - ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D - and F inoculum (P < 0.05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D - were the lowest ( - 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D - animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D − ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D − and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D − were the lowest ( − 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D − animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D - ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D - and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D - were the lowest ( - 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D - animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. Understanding the interactions between hydrogen producers and consumers in the rumen ecosystem is important for ruminant production and methane mitigation. The present study explored the relationships between rumen protozoa, methanogens and fermentation characteristics. A total of six donor sheep harbouring (F, faunated) or not (D, defaunated) protozoa in their rumens (D animals were kept without protozoa for a period of a few months (D - ) or for more than 2 years (D+)) were used in in vitro and in vivo experiments. In vitro the absence of protozoa decreased NH3 and butyrate production and had no effect on methane. In contrast, the liquid-associated bacterial and methanogens fraction of D+ inocula produced more methane than D - and F inoculum (P < 0·05). In vivo fermentation parameters of donor animals showed the same trend on NH3 and butyrate and showed that D+ animals were high methane emitters, while D - were the lowest ( - 35 %). The concentration of dissolved dihydrogen measured after feeding followed the opposite trend. Methane emissions did not correlate with the relative abundance of methanogens in the rumen measured by quantitative PCR, but there was a trend for higher methanogens concentration in the solid-associated population of D+ animals compared with D - animals. In contrast, PCR-denaturing gradient gel electrophoresis profiles of methanogens' methyl coenzyme-M reductase A gene showed a clear clustering in liquid-associated fractions for all three groups of donors but fewer differences in solid-associated fractions. These results show that the absence of protozoa may affect differently the methanogen community and methane emissions in wethers. |
Author | Jouany, Jean-Pierre Martin, Cécile Morgavi, Diego P. Ranilla, Maria José |
Author_xml | – sequence: 1 givenname: Diego P. surname: Morgavi fullname: Morgavi, Diego P. email: diego.morgavi@clermont.inra.fr organization: INRA, UR1213 Herbivores, Site de Theix, F-63122 St-Genès-Champanelle, France – sequence: 2 givenname: Cécile surname: Martin fullname: Martin, Cécile organization: INRA, UR1213 Herbivores, Site de Theix, F-63122 St-Genès-Champanelle, France – sequence: 3 givenname: Jean-Pierre surname: Jouany fullname: Jouany, Jean-Pierre organization: INRA, UR1213 Herbivores, Site de Theix, F-63122 St-Genès-Champanelle, France – sequence: 4 givenname: Maria José surname: Ranilla fullname: Ranilla, Maria José organization: Departamento de Producción Animal, Universidad de León, 24071 León, Spain |
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ContentType | Journal Article |
Copyright | Copyright © The Authors 2011 2015 INIST-CNRS Distributed under a Creative Commons Attribution 4.0 International License |
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DocumentTitleAlternate | D. P. Morgavi et al. Rumen protozoa and the methanogen community |
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Keywords | Rumen protozoa Methane production Fermentation characteristics Methanogens Methane Stomach Vertebrata Mammalia Digestive system Rumen Fermentation methane production methanogène rumen protozoa methanogens fermentation characteristics |
Language | English |
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References | Forster (S0007114511002935_ref3) 2007 Goering (S0007114511002935_ref18) 1970 Martin (S0007114511002935_ref42) 2007 Demeyer (S0007114511002935_ref38) 1991 S0007114511002935_ref39 S0007114511002935_ref33 S0007114511002935_ref34 S0007114511002935_ref36 Robinson (S0007114511002935_ref37) 1981; 41 S0007114511002935_ref31 Davies (S0007114511002935_ref35) 1965 S0007114511002935_ref19 S0007114511002935_ref26 S0007114511002935_ref28 S0007114511002935_ref29 S0007114511002935_ref22 Savelkoul (S0007114511002935_ref30) 1999; 37 S0007114511002935_ref23 S0007114511002935_ref24 S0007114511002935_ref25 S0007114511002935_ref20 S0007114511002935_ref21 Ogimoto (S0007114511002935_ref32) 1981 Muyzer (S0007114511002935_ref27) 1993; 59 Thauer (S0007114511002935_ref51) 1977; 41 S0007114511002935_ref2 S0007114511002935_ref5 S0007114511002935_ref4 S0007114511002935_ref7 S0007114511002935_ref6 S0007114511002935_ref15 S0007114511002935_ref16 S0007114511002935_ref17 S0007114511002935_ref11 S0007114511002935_ref55 S0007114511002935_ref12 S0007114511002935_ref13 S0007114511002935_ref14 S0007114511002935_ref52 S0007114511002935_ref53 S0007114511002935_ref54 S0007114511002935_ref10 S0007114511002935_ref50 Hungate (S0007114511002935_ref49) 1967; 59 Steinfeld (S0007114511002935_ref1) 2006 S0007114511002935_ref9 S0007114511002935_ref48 S0007114511002935_ref8 S0007114511002935_ref44 S0007114511002935_ref45 S0007114511002935_ref46 S0007114511002935_ref47 S0007114511002935_ref40 S0007114511002935_ref41 S0007114511002935_ref43 |
References_xml | – ident: S0007114511002935_ref9 doi: 10.1071/EA07298 – ident: S0007114511002935_ref2 doi: 10.1071/EA07220 – volume: 41 start-page: 100 year: 1977 ident: S0007114511002935_ref51 article-title: Energy conservation in chemotrophic anaerobic bacteria publication-title: Microbiol Mol Biol Rev contributor: fullname: Thauer – ident: S0007114511002935_ref14 doi: 10.1139/m93-009 – ident: S0007114511002935_ref39 doi: 10.1099/ijs.0.65394-0 – ident: S0007114511002935_ref25 doi: 10.1038/nprot.2008.73 – ident: S0007114511002935_ref55 doi: 10.1016/S0378-1097(04)00045-X – ident: S0007114511002935_ref29 doi: 10.1046/j.1462-2920.2002.00358.x – ident: S0007114511002935_ref53 doi: 10.1079/BJN19820013 – ident: S0007114511002935_ref17 doi: 10.1051/rnd:19790507 – ident: S0007114511002935_ref23 doi: 10.1111/j.1574-6941.2007.00413.x – ident: S0007114511002935_ref20 doi: 10.2527/jas.2007-0774 – ident: S0007114511002935_ref54 doi: 10.1016/j.ics.2006.01.019 – ident: S0007114511002935_ref19 doi: 10.1021/es00051a025 – ident: S0007114511002935_ref28 doi: 10.1016/j.mimet.2003.12.006 – start-page: 294 year: 1965 ident: S0007114511002935_ref35 article-title: Application of the autoanalyser in a river authority laboratory publication-title: Symposium Technicon contributor: fullname: Davies – ident: S0007114511002935_ref4 doi: 10.1126/science.1174760 – ident: S0007114511002935_ref43 doi: 10.1016/j.livsci.2009.12.011 – ident: S0007114511002935_ref48 doi: 10.1007/978-1-4612-2776-2 – ident: S0007114511002935_ref22 doi: 10.1111/j.1574-6941.2007.00392.x – ident: S0007114511002935_ref41 doi: 10.1079/BJN2003932 – volume: 59 start-page: 695 year: 1993 ident: S0007114511002935_ref27 article-title: Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA publication-title: Appl Environ Microbiol doi: 10.1128/AEM.59.3.695-700.1993 contributor: fullname: Muyzer – ident: S0007114511002935_ref52 doi: 10.1111/j.1574-6968.1994.tb06758.x – ident: S0007114511002935_ref6 doi: 10.4141/A03-109 – ident: S0007114511002935_ref11 doi: 10.1128/AEM.02453-08 – ident: S0007114511002935_ref8 doi: 10.1051/rnd:2003005 – volume-title: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change year: 2007 ident: S0007114511002935_ref3 contributor: fullname: Forster – ident: S0007114511002935_ref16 doi: 10.1016/j.anifeedsci.2010.07.002 – ident: S0007114511002935_ref7 doi: 10.1071/AR99008 – ident: S0007114511002935_ref44 doi: 10.2527/jas.2005-652 – ident: S0007114511002935_ref33 doi: 10.1021/jf034505v – volume: 59 start-page: 158 year: 1967 ident: S0007114511002935_ref49 article-title: Hydrogen as an intermediate in the rumen fermentation publication-title: Arch Microbiol contributor: fullname: Hungate – volume-title: Forage Fibre Analysis year: 1970 ident: S0007114511002935_ref18 contributor: fullname: Goering – ident: S0007114511002935_ref31 doi: 10.1093/nar/21.13.3021 – start-page: 390 volume-title: Livestock's Long Shadow Environmental Issues and Options year: 2006 ident: S0007114511002935_ref1 contributor: fullname: Steinfeld – ident: S0007114511002935_ref5 doi: 10.1017/S1751731110000546 – ident: S0007114511002935_ref21 doi: 10.1111/j.1574-6941.2007.00394.x – ident: S0007114511002935_ref13 doi: 10.2527/jas.2010-2947 – ident: S0007114511002935_ref34 doi: 10.1021/ac60252a045 – ident: S0007114511002935_ref46 doi: 10.1071/EA07236 – volume-title: Atlas of Rumen Microbiology year: 1981 ident: S0007114511002935_ref32 contributor: fullname: Ogimoto – ident: S0007114511002935_ref40 doi: 10.3168/jds.2008-1903 – ident: S0007114511002935_ref47 doi: 10.1111/j.1472-765X.1995.tb01048.x – volume: 37 start-page: 3083 year: 1999 ident: S0007114511002935_ref30 article-title: Amplified-fragment length polymorphism analysis: the state of an art publication-title: J Clin Microbiol doi: 10.1128/JCM.37.10.3083-3091.1999 contributor: fullname: Savelkoul – ident: S0007114511002935_ref50 doi: 10.1007/BF00394043 – ident: S0007114511002935_ref12 doi: 10.1016/S0301-6226(03)00117-9 – ident: S0007114511002935_ref24 doi: 10.1111/j.1574-6941.2006.00190.x – volume: 41 start-page: 545 year: 1981 ident: S0007114511002935_ref37 article-title: Method for measuring dissolved hydrogen in anaerobic ecosystems: application to the rumen publication-title: Appl Environ Microbiol doi: 10.1128/AEM.41.2.545-548.1981 contributor: fullname: Robinson – ident: S0007114511002935_ref26 doi: 10.1099/00221287-148-11-3521 – ident: S0007114511002935_ref10 doi: 10.1017/S0007114508981435 – ident: S0007114511002935_ref15 doi: 10.1007/s00284-005-0266-9 – start-page: 217 volume-title: Rumen Microbial Metabolism and Ruminant Digestion year: 1991 ident: S0007114511002935_ref38 contributor: fullname: Demeyer – start-page: 609 volume-title: Energy and Protein Metabolism and Nutrition, EAAP Publication year: 2007 ident: S0007114511002935_ref42 contributor: fullname: Martin – ident: S0007114511002935_ref36 doi: 10.1016/S0377-8401(98)00239-9 – ident: S0007114511002935_ref45 doi: 10.1111/j.1472-765X.2007.02251.x |
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SubjectTerms | Ammonia Animals Animals, Inbred Strains Archaeal Proteins - genetics Archaeal Proteins - metabolism Biological and medical sciences Cause-effect relationships Digestion Emissions Enzymes Euryarchaeota - enzymology Euryarchaeota - isolation & purification Euryarchaeota - physiology Feeding. Feeding behavior Fermentation Food and Nutrition Fundamental and applied biological sciences. Psychology Gastrointestinal Contents - chemistry Gastrointestinal Contents - microbiology Gastrointestinal Contents - parasitology Gram-Negative Bacteria - isolation & purification Gram-Negative Bacteria - metabolism Gram-Positive Bacteria - isolation & purification Gram-Positive Bacteria - metabolism Life Sciences Male Manures Metagenome Methane Methane - metabolism Methanogenesis Microbiology Oxidoreductases - genetics Oxidoreductases - metabolism Postprandial Period Protozoa Relative abundance Rumen - microbiology Rumen - parasitology Ruminantia Sheep, Domestic - microbiology Sheep, Domestic - parasitology Sheep, Domestic - physiology Specific Pathogen-Free Organisms Symbiosis Vertebrates: anatomy and physiology, studies on body, several organs or systems |
Title | Rumen protozoa and methanogenesis: not a simple cause–effect relationship |
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