Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host
Abstract Background Producing animal protein while reducing the animal’s impact on the environment, e.g., through improved feed efficiency and lowered methane emissions, has gained interest in recent years. Genetic selection is one possible path to reduce the environmental impact of livestock produc...
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-023-09660-3 |
| _version_ | 1827635472324624384 |
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| author | Melanie K. Hess Hannah E. Hodgkinson Andrew S. Hess Larissa Zetouni Juliana C. C. Budel Hannah Henry Alistair Donaldson Timothy P. Bilton Tracey C. van Stijn Michelle R. Kirk Ken G. Dodds Rudiger Brauning Alan F. McCulloch Sharon M. Hickey Patricia L. Johnson Arjan Jonker Nickolas Morton Shaun Hendy V. Hutton Oddy Peter H. Janssen John C. McEwan Suzanne J. Rowe |
| author_facet | Melanie K. Hess Hannah E. Hodgkinson Andrew S. Hess Larissa Zetouni Juliana C. C. Budel Hannah Henry Alistair Donaldson Timothy P. Bilton Tracey C. van Stijn Michelle R. Kirk Ken G. Dodds Rudiger Brauning Alan F. McCulloch Sharon M. Hickey Patricia L. Johnson Arjan Jonker Nickolas Morton Shaun Hendy V. Hutton Oddy Peter H. Janssen John C. McEwan Suzanne J. Rowe |
| author_sort | Melanie K. Hess |
| collection | DOAJ |
| description | Abstract Background Producing animal protein while reducing the animal’s impact on the environment, e.g., through improved feed efficiency and lowered methane emissions, has gained interest in recent years. Genetic selection is one possible path to reduce the environmental impact of livestock production, but these traits are difficult and expensive to measure on many animals. The rumen microbiome may serve as a proxy for these traits due to its role in feed digestion. Restriction enzyme-reduced representation sequencing (RE-RRS) is a high-throughput and cost-effective approach to rumen metagenome profiling, but the systematic (e.g., sequencing) and biological factors influencing the resulting reference based (RB) and reference free (RF) profiles need to be explored before widespread industry adoption is possible. Results Metagenome profiles were generated by RE-RRS of 4,479 rumen samples collected from 1,708 sheep, and assigned to eight groups based on diet, age, time off feed, and country (New Zealand or Australia) at the time of sample collection. Systematic effects were found to have minimal influence on metagenome profiles. Diet was a major driver of differences between samples, followed by time off feed, then age of the sheep. The RF approach resulted in more reads being assigned per sample and afforded greater resolution when distinguishing between groups than the RB approach. Normalizing relative abundances within the sampling Cohort abolished structures related to age, diet, and time off feed, allowing a clear signal based on methane emissions to be elucidated. Genus-level abundances of rumen microbes showed low-to-moderate heritability and repeatability and were consistent between diets. Conclusions Variation in rumen metagenomic profiles was influenced by diet, age, time off feed and genetics. Not accounting for environmental factors may limit the ability to associate the profile with traits of interest. However, these differences can be accounted for by adjusting for Cohort effects, revealing robust biological signals. The abundances of some genera were consistently heritable and repeatable across different environments, suggesting that metagenomic profiles could be used to predict an individual’s future performance, or performance of its offspring, in a range of environments. These results highlight the potential of using rumen metagenomic profiles for selection purposes in a practical, agricultural setting. |
| first_indexed | 2024-03-09T15:28:11Z |
| format | Article |
| id | doaj.art-559e06adc5ae47308edd263d5a51d77e |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-09T15:28:11Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-559e06adc5ae47308edd263d5a51d77e2023-11-26T12:25:36ZengBMCBMC Genomics1471-21642023-09-0124112610.1186/s12864-023-09660-3Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the hostMelanie K. Hess0Hannah E. Hodgkinson1Andrew S. Hess2Larissa Zetouni3Juliana C. C. Budel4Hannah Henry5Alistair Donaldson6Timothy P. Bilton7Tracey C. van Stijn8Michelle R. Kirk9Ken G. Dodds10Rudiger Brauning11Alan F. McCulloch12Sharon M. Hickey13Patricia L. Johnson14Arjan Jonker15Nickolas Morton16Shaun Hendy17V. Hutton Oddy18Peter H. Janssen19John C. McEwan20Suzanne J. Rowe21AgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreNSW Department of Primary Industries, University of New EnglandAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Grasslands Research CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Ruakura Research CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Grasslands Research CentreTe Pūnaha Matatini, University of AucklandTe Pūnaha Matatini, University of AucklandNSW Department of Primary Industries, University of New EnglandAgResearch Ltd., Grasslands Research CentreAgResearch Ltd., Invermay Agricultural CentreAgResearch Ltd., Invermay Agricultural CentreAbstract Background Producing animal protein while reducing the animal’s impact on the environment, e.g., through improved feed efficiency and lowered methane emissions, has gained interest in recent years. Genetic selection is one possible path to reduce the environmental impact of livestock production, but these traits are difficult and expensive to measure on many animals. The rumen microbiome may serve as a proxy for these traits due to its role in feed digestion. Restriction enzyme-reduced representation sequencing (RE-RRS) is a high-throughput and cost-effective approach to rumen metagenome profiling, but the systematic (e.g., sequencing) and biological factors influencing the resulting reference based (RB) and reference free (RF) profiles need to be explored before widespread industry adoption is possible. Results Metagenome profiles were generated by RE-RRS of 4,479 rumen samples collected from 1,708 sheep, and assigned to eight groups based on diet, age, time off feed, and country (New Zealand or Australia) at the time of sample collection. Systematic effects were found to have minimal influence on metagenome profiles. Diet was a major driver of differences between samples, followed by time off feed, then age of the sheep. The RF approach resulted in more reads being assigned per sample and afforded greater resolution when distinguishing between groups than the RB approach. Normalizing relative abundances within the sampling Cohort abolished structures related to age, diet, and time off feed, allowing a clear signal based on methane emissions to be elucidated. Genus-level abundances of rumen microbes showed low-to-moderate heritability and repeatability and were consistent between diets. Conclusions Variation in rumen metagenomic profiles was influenced by diet, age, time off feed and genetics. Not accounting for environmental factors may limit the ability to associate the profile with traits of interest. However, these differences can be accounted for by adjusting for Cohort effects, revealing robust biological signals. The abundances of some genera were consistently heritable and repeatable across different environments, suggesting that metagenomic profiles could be used to predict an individual’s future performance, or performance of its offspring, in a range of environments. These results highlight the potential of using rumen metagenomic profiles for selection purposes in a practical, agricultural setting.https://doi.org/10.1186/s12864-023-09660-3Genotyping-by-sequencingRestriction enzyme reduced representation sequencingRumen microbiomeMetagenomeGeneticsReference based |
| spellingShingle | Melanie K. Hess Hannah E. Hodgkinson Andrew S. Hess Larissa Zetouni Juliana C. C. Budel Hannah Henry Alistair Donaldson Timothy P. Bilton Tracey C. van Stijn Michelle R. Kirk Ken G. Dodds Rudiger Brauning Alan F. McCulloch Sharon M. Hickey Patricia L. Johnson Arjan Jonker Nickolas Morton Shaun Hendy V. Hutton Oddy Peter H. Janssen John C. McEwan Suzanne J. Rowe Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host BMC Genomics Genotyping-by-sequencing Restriction enzyme reduced representation sequencing Rumen microbiome Metagenome Genetics Reference based |
| title | Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| title_full | Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| title_fullStr | Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| title_full_unstemmed | Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| title_short | Large-scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| title_sort | large scale analysis of sheep rumen metagenome profiles captured by reduced representation sequencing reveals individual profiles are influenced by the environment and genetics of the host |
| topic | Genotyping-by-sequencing Restriction enzyme reduced representation sequencing Rumen microbiome Metagenome Genetics Reference based |
| url | https://doi.org/10.1186/s12864-023-09660-3 |
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