A unified compendium of prokaryotic and viral genomes from over 300 anaerobic digestion microbiomes

IF 6.2 2区 环境科学与生态学 Q1 GENETICS & HEREDITY Environmental Microbiome Pub Date : 2024-01-02 DOI:10.1186/s40793-023-00545-2
Victor Borin Centurion, Alessandro Rossi, Esteban Orellana, Gabriele Ghiotto, Balázs Kakuk, Maria Silvia Morlino, Arianna Basile, Guido Zampieri, Laura Treu, Stefano Campanaro
{"title":"A unified compendium of prokaryotic and viral genomes from over 300 anaerobic digestion microbiomes","authors":"Victor Borin Centurion, Alessandro Rossi, Esteban Orellana, Gabriele Ghiotto, Balázs Kakuk, Maria Silvia Morlino, Arianna Basile, Guido Zampieri, Laura Treu, Stefano Campanaro","doi":"10.1186/s40793-023-00545-2","DOIUrl":null,"url":null,"abstract":"The anaerobic digestion process degrades organic matter into simpler compounds and occurs in strictly anaerobic and microaerophilic environments. The process is carried out by a diverse community of microorganisms where each species has a unique role and it has relevant biotechnological applications since it is used for biogas production. Some aspects of the microbiome, including its interaction with phages, remains still unclear: a better comprehension of the community composition and role of each species is crucial for a cured understanding of the carbon cycle in anaerobic systems and improving biogas production. The primary objective of this study was to expand our understanding on the anaerobic digestion microbiome by jointly analyzing its prokaryotic and viral components. By integrating 192 additional datasets into a previous metagenomic database, the binning process generated 11,831 metagenome-assembled genomes from 314 metagenome samples published between 2014 and 2022, belonging to 4,568 non-redundant species based on ANI calculation and quality verification. CRISPR analysis on these genomes identified 76 archaeal genomes with active phage interactions. Moreover, single-nucleotide variants further pointed to archaea as the most critical members of the community. Among the MAGs, two methanogenic archaea, Methanothrix sp. 43zhSC_152 and Methanoculleus sp. 52maCN_3230, had the highest number of SNVs, with the latter having almost double the density of most other MAGs. This study offers a more comprehensive understanding of microbial community structures that thrive at different temperatures. The findings revealed that the fraction of archaeal species characterized at the genome level and reported in public databases is higher than that of bacteria, although still quite limited. The identification of shared spacers between phages and microbes implies a history of phage-bacterial interactions, and specifically lysogenic infections. A significant number of SNVs were identified, primarily comprising synonymous and nonsynonymous variants. Together, the findings indicate that methanogenic archaea are subject to intense selective pressure and suggest that genomic variants play a critical role in the anaerobic digestion process. Overall, this study provides a more balanced and diverse representation of the anaerobic digestion microbiota in terms of geographic location, temperature range and feedstock utilization.","PeriodicalId":48553,"journal":{"name":"Environmental Microbiome","volume":"7 1","pages":""},"PeriodicalIF":6.2000,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Environmental Microbiome","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1186/s40793-023-00545-2","RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"GENETICS & HEREDITY","Score":null,"Total":0}
引用次数: 0

Abstract

The anaerobic digestion process degrades organic matter into simpler compounds and occurs in strictly anaerobic and microaerophilic environments. The process is carried out by a diverse community of microorganisms where each species has a unique role and it has relevant biotechnological applications since it is used for biogas production. Some aspects of the microbiome, including its interaction with phages, remains still unclear: a better comprehension of the community composition and role of each species is crucial for a cured understanding of the carbon cycle in anaerobic systems and improving biogas production. The primary objective of this study was to expand our understanding on the anaerobic digestion microbiome by jointly analyzing its prokaryotic and viral components. By integrating 192 additional datasets into a previous metagenomic database, the binning process generated 11,831 metagenome-assembled genomes from 314 metagenome samples published between 2014 and 2022, belonging to 4,568 non-redundant species based on ANI calculation and quality verification. CRISPR analysis on these genomes identified 76 archaeal genomes with active phage interactions. Moreover, single-nucleotide variants further pointed to archaea as the most critical members of the community. Among the MAGs, two methanogenic archaea, Methanothrix sp. 43zhSC_152 and Methanoculleus sp. 52maCN_3230, had the highest number of SNVs, with the latter having almost double the density of most other MAGs. This study offers a more comprehensive understanding of microbial community structures that thrive at different temperatures. The findings revealed that the fraction of archaeal species characterized at the genome level and reported in public databases is higher than that of bacteria, although still quite limited. The identification of shared spacers between phages and microbes implies a history of phage-bacterial interactions, and specifically lysogenic infections. A significant number of SNVs were identified, primarily comprising synonymous and nonsynonymous variants. Together, the findings indicate that methanogenic archaea are subject to intense selective pressure and suggest that genomic variants play a critical role in the anaerobic digestion process. Overall, this study provides a more balanced and diverse representation of the anaerobic digestion microbiota in terms of geographic location, temperature range and feedstock utilization.
查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
来自 300 多个厌氧消化微生物组的原核生物和病毒基因组统一汇编
厌氧消化过程将有机物降解为较简单的化合物,发生在严格厌氧和微嗜水的环境中。厌氧消化过程由多种多样的微生物群落进行,其中每个物种都有独特的作用,而且厌氧消化还具有相关的生物技术应用,因为它可用于生产沼气。微生物群的某些方面,包括其与噬菌体的相互作用,仍不清楚:更好地理解群落组成和每个物种的作用,对于深入了解厌氧系统中的碳循环和提高沼气产量至关重要。本研究的主要目的是通过联合分析厌氧消化微生物群的原核生物和病毒成分,扩大我们对厌氧消化微生物群的了解。通过将 192 个附加数据集整合到之前的元基因组数据库中,分选过程从 2014 年至 2022 年间发表的 314 个元基因组样本中生成了 11831 个元基因组组装基因组,根据 ANI 计算和质量验证,这些基因组属于 4568 个非冗余物种。对这些基因组进行的CRISPR分析发现了76个具有活跃噬菌体相互作用的古菌基因组。此外,单核苷酸变异进一步表明古菌是群落中最关键的成员。在这些噬菌体中,两个产甲烷古细菌--Methanothrix sp.(43zhSC_152)和 Methanoculleus sp.(52maCN_3230)--的 SNV 数量最多,其中后者的 SNV 密度几乎是大多数其他噬菌体的两倍。这项研究让人们对在不同温度下生长的微生物群落结构有了更全面的了解。研究结果表明,在基因组水平上表征并在公共数据库中报告的古细菌物种的比例高于细菌,但仍然相当有限。噬菌体与微生物之间共享间隔的发现意味着噬菌体与细菌之间存在相互作用的历史,特别是溶菌感染。研究发现了大量 SNVs,主要包括同义和非同义变异。这些发现共同表明,产甲烷古细菌承受着巨大的选择压力,并表明基因组变异在厌氧消化过程中发挥着关键作用。总之,这项研究从地理位置、温度范围和原料利用等方面提供了厌氧消化微生物群更加平衡和多样化的代表。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Environmental Microbiome
Environmental Microbiome Immunology and Microbiology-Microbiology
CiteScore
7.40
自引率
2.50%
发文量
55
审稿时长
13 weeks
期刊介绍: Microorganisms, omnipresent across Earth's diverse environments, play a crucial role in adapting to external changes, influencing Earth's systems and cycles, and contributing significantly to agricultural practices. Through applied microbiology, they offer solutions to various everyday needs. Environmental Microbiome recognizes the universal presence and significance of microorganisms, inviting submissions that explore the diverse facets of environmental and applied microbiological research.
期刊最新文献
Exploring the biosynthesis potential of permafrost microbiomes. Soil properties drive nitrous oxide accumulation patterns by shaping denitrifying bacteriomes. Metatranscriptomics of microbial biofilm succession on HDPE foil: uncovering plastic-degrading potential in soil communities. Stochasticity-dominated rare fungal endophytes contribute to coexistence stability and saponin accumulation in Panax species. Selenium alters the gene content but not the taxonomic composition of the soil microbiome.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1