Begmatov Shahjahon, Beletsky Alexey V, Mardanov Andrey V, Lukina Anastasia P, Glukhova Liubov B, Karnachuk Olga V, Ravin Nikolai V
Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia.
Tomsk State University, Tomsk, Russia.
mSphere. 2025 Jul 29;10(7):e0029425. doi: 10.1128/msphere.00294-25. Epub 2025 Jun 30.
Genome reduction and associated metabolic deficiencies have been described in various lineages of parasitic and symbiotic microorganisms that obtain essential nutrients from their partners, and in some free-living microorganisms that inhabit stable environments. The animal gut is a relatively stable ecosystem, characterized by an abundance of organic substances and a high concentration of microorganisms, which provides favorable conditions for the survival of microorganisms with reduced genomes. Metagenomic analysis of 49 samples of feces of farm animals (cows, sheep, yaks, and horses) revealed uncultured lineages of bacteria with reduced genomes (<1 Mbp): family UBA1242 (, ), order Rs-D84 (), and family UBA9783 (, ), defined in genome-taxonomy database. Analysis of the genomes showed that these bacteria lacked pathways for the biosynthesis of amino acids, nucleotides, lipids, and many other essential metabolites. The UBA9783 genomes encoded a near-complete Embden-Meyerhof glycolytic pathway and the non-oxidative phase of the pentose phosphate pathway, while in UBA1242 and Rs-D84, these pathways are incomplete. All bacteria are limited to fermentative metabolism and lack aerobic and anaerobic respiratory pathways. All UBA9783 and some Rs-D84 genomes encoded FF-type ATP synthase and pyrophosphate-energized proton pump; they also can import and utilize peptides and some amino acids. While UBA9783 bacteria could thrive as specialized free-living organisms in the organic-rich gut environment, the UBA1242 and Rs-D84 lineages appear to have adopted the lifestyle of an obligate symbiont/parasite, obtaining metabolites from other cells.IMPORTANCEThe microbiota of the animal gastrointestinal tracts is a complex community of microorganisms which interact in a synergistic or antagonistic relationship and play key nutritional and metabolic roles. However, despite its importance, the gut microbiota of farm animals, especially its uncultured majority, remains largely unexplored. We performed a metagenomic analysis of the gut microbiome of farm animals and characterized three uncultured lineages of bacteria with reduced genomes (<1 Mbp) from the phyla , , and . These bacteria were predicted to possess key metabolic deficiencies such as the inability to synthesize essential cell metabolites, suggesting their adaptation to the lifestyle of a symbiont/parasite, or a scavenger obtaining nutrients from the organic-rich gut environment. This study shows that genome reduction with metabolic specialization and adaptation to a partner-dependent lifestyle occurred through convergent evolution in several phylogenetically distant lineages of gut microbiota.
在从宿主获取必需营养的各种寄生和共生微生物谱系中，以及在一些栖息于稳定环境的自由生活微生物中，都有基因组缩减及相关代谢缺陷的描述。动物肠道是一个相对稳定的生态系统，其特点是含有丰富的有机物质和高浓度的微生物，这为基因组缩减的微生物生存提供了有利条件。对49份农场动物（牛、羊、牦牛和马）粪便样本进行的宏基因组分析揭示了基因组缩减（<1 Mbp）的未培养细菌谱系：UBA1242科（，）、Rs - D84目（）和UBA9783科（，），这些在基因组分类数据库中已有定义。对这些基因组的分析表明，这些细菌缺乏氨基酸、核苷酸、脂质和许多其他必需代谢物的生物合成途径。UBA9783基因组编码了近乎完整的糖酵解途径和磷酸戊糖途径的非氧化阶段，而在UBA1242和Rs - D84中，这些途径是不完整的。所有细菌都局限于发酵代谢，缺乏有氧和无氧呼吸途径。所有UBA9783和一些Rs - D84基因组编码了FF型ATP合酶和焦磷酸驱动的质子泵；它们还可以导入和利用肽及一些氨基酸。虽然UBA9783细菌可以在富含有机物的肠道环境中作为特殊的自由生活生物茁壮成长，但UBA1242和Rs - D84谱系似乎已经采用了专性共生体/寄生虫的生活方式，从其他细胞获取代谢物。
重要性
动物胃肠道的微生物群是一个复杂的微生物群落，它们以协同或拮抗关系相互作用，并发挥关键的营养和代谢作用。然而，尽管其很重要，但农场动物的肠道微生物群，尤其是其中未培养的大多数，在很大程度上仍未被探索。我们对农场动物的肠道微生物组进行了宏基因组分析，并对来自门、和的三个基因组缩减（<1 Mbp）的未培养细菌谱系进行了表征。预计这些细菌具有关键的代谢缺陷，如无法合成必需的细胞代谢物，这表明它们适应了共生体/寄生虫的生活方式，或者是从富含有机物的肠道环境中获取营养的清道夫。这项研究表明，在肠道微生物群的几个系统发育距离较远的谱系中，通过趋同进化发生了基因组缩减以及代谢特化和对依赖伙伴生活方式的适应。
