Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens
Abstract Background Viruses are the most abundant biological entities on Earth, known to be crucial components of microbial ecosystems. However, there is little information on the viral community within agricultural waste. There are currently ~ 2.7 million dairy cattle in the UK producing 7–8% of th...
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doaj-53b7c81d7f394e3cb1b27d9e2d8551a02021-03-21T12:48:45ZengBMCMicrobiome2049-26182021-03-019111710.1186/s40168-021-01010-3Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogensRyan Cook0Steve Hooton1Urmi Trivedi2Liz King3Christine E. R. Dodd4Jon L. Hobman5Dov J. Stekel6Michael A. Jones7Andrew D. Millard8School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington CampusSchool of Biosciences, University of Nottingham, Sutton Bonington CampusEdinburgh Genomics, School of Biological Sciences, University of EdinburghSchool of Biosciences, University of Nottingham, Sutton Bonington CampusSchool of Biosciences, University of Nottingham, Sutton Bonington CampusSchool of Biosciences, University of Nottingham, Sutton Bonington CampusSchool of Biosciences, University of Nottingham, Sutton Bonington CampusSchool of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington CampusDept Genetics and Genome Biology, University of LeicesterAbstract Background Viruses are the most abundant biological entities on Earth, known to be crucial components of microbial ecosystems. However, there is little information on the viral community within agricultural waste. There are currently ~ 2.7 million dairy cattle in the UK producing 7–8% of their own bodyweight in manure daily, and 28 million tonnes annually. To avoid pollution of UK freshwaters, manure must be stored and spread in accordance with guidelines set by DEFRA. Manures are used as fertiliser, and widely spread over crop fields, yet little is known about their microbial composition. We analysed the virome of agricultural slurry over a 5-month period using short and long-read sequencing. Results Hybrid sequencing uncovered more high-quality viral genomes than long or short-reads alone; yielding 7682 vOTUs, 174 of which were complete viral genomes. The slurry virome was highly diverse and dominated by lytic bacteriophage, the majority of which represent novel genera (~ 98%). Despite constant influx and efflux of slurry, the composition and diversity of the slurry virome was extremely stable over time, with 55% of vOTUs detected in all samples over a 5-month period. Functional annotation revealed a diverse and abundant range of auxiliary metabolic genes and novel features present in the community, including the agriculturally relevant virulence factor VapE, which was widely distributed across different phage genera that were predicted to infect several hosts. Furthermore, we identified an abundance of phage-encoded diversity-generating retroelements, which were previously thought to be rare on lytic viral genomes. Additionally, we identified a group of crAssphages, including lineages that were previously thought only to be found in the human gut. Conclusions The cattle slurry virome is complex, diverse and dominated by novel genera, many of which are not recovered using long or short-reads alone. Phages were found to encode a wide range of AMGs that are not constrained to particular groups or predicted hosts, including virulence determinants and putative ARGs. The application of agricultural slurry to land may therefore be a driver of bacterial virulence and antimicrobial resistance in the environment. Video abstracthttps://doi.org/10.1186/s40168-021-01010-3PhagesViromicsVapEDiversity-generating retroelementscrAssphagePromethION |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ryan Cook Steve Hooton Urmi Trivedi Liz King Christine E. R. Dodd Jon L. Hobman Dov J. Stekel Michael A. Jones Andrew D. Millard |
spellingShingle |
Ryan Cook Steve Hooton Urmi Trivedi Liz King Christine E. R. Dodd Jon L. Hobman Dov J. Stekel Michael A. Jones Andrew D. Millard Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens Microbiome Phages Viromics VapE Diversity-generating retroelements crAssphage PromethION |
author_facet |
Ryan Cook Steve Hooton Urmi Trivedi Liz King Christine E. R. Dodd Jon L. Hobman Dov J. Stekel Michael A. Jones Andrew D. Millard |
author_sort |
Ryan Cook |
title |
Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
title_short |
Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
title_full |
Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
title_fullStr |
Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
title_full_unstemmed |
Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
title_sort |
hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2021-03-01 |
description |
Abstract Background Viruses are the most abundant biological entities on Earth, known to be crucial components of microbial ecosystems. However, there is little information on the viral community within agricultural waste. There are currently ~ 2.7 million dairy cattle in the UK producing 7–8% of their own bodyweight in manure daily, and 28 million tonnes annually. To avoid pollution of UK freshwaters, manure must be stored and spread in accordance with guidelines set by DEFRA. Manures are used as fertiliser, and widely spread over crop fields, yet little is known about their microbial composition. We analysed the virome of agricultural slurry over a 5-month period using short and long-read sequencing. Results Hybrid sequencing uncovered more high-quality viral genomes than long or short-reads alone; yielding 7682 vOTUs, 174 of which were complete viral genomes. The slurry virome was highly diverse and dominated by lytic bacteriophage, the majority of which represent novel genera (~ 98%). Despite constant influx and efflux of slurry, the composition and diversity of the slurry virome was extremely stable over time, with 55% of vOTUs detected in all samples over a 5-month period. Functional annotation revealed a diverse and abundant range of auxiliary metabolic genes and novel features present in the community, including the agriculturally relevant virulence factor VapE, which was widely distributed across different phage genera that were predicted to infect several hosts. Furthermore, we identified an abundance of phage-encoded diversity-generating retroelements, which were previously thought to be rare on lytic viral genomes. Additionally, we identified a group of crAssphages, including lineages that were previously thought only to be found in the human gut. Conclusions The cattle slurry virome is complex, diverse and dominated by novel genera, many of which are not recovered using long or short-reads alone. Phages were found to encode a wide range of AMGs that are not constrained to particular groups or predicted hosts, including virulence determinants and putative ARGs. The application of agricultural slurry to land may therefore be a driver of bacterial virulence and antimicrobial resistance in the environment. Video abstract |
topic |
Phages Viromics VapE Diversity-generating retroelements crAssphage PromethION |
url |
https://doi.org/10.1186/s40168-021-01010-3 |
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