Metaproteogenomics resolution of a high-CO2 aquifer community reveals a complex cellular adaptation of groundwater Gracilibacteria to a host-dependent lifestyle.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY
Perla Abigail Figueroa-Gonzalez, Till L V Bornemann, Tjorven Hinzke, Sandra Maaß, Anke Trautwein-Schult, Joern Starke, Carrie J Moore, Sarah P Esser, Julia Plewka, Tobias Hesse, Torsten C Schmidt, Ulrich Schreiber, Batbileg Bor, Dörte Becher, Alexander J Probst
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引用次数: 0

Abstract

Background: Bacteria of the candidate phyla radiation (CPR), constituting about 25% of the bacterial biodiversity, are characterized by small cell size and patchy genomes without complete key metabolic pathways, suggesting a symbiotic lifestyle. Gracilibacteria (BD1-5), which are part of the CPR branch, possess alternate coded genomes and have not yet been cultivated. The lifestyle of Gracilibacteria, their temporal dynamics, and activity in natural ecosystems, particularly in groundwater, has remained largely unexplored. Here, we aimed to investigate Gracilibacteria activity in situ and to discern their lifestyle based on expressed genes, using the metaproteogenome of Gracilibacteria as a function of time in the cold-water geyser Wallender Born in the Volcanic Eifel region in Germany.

Results: We coupled genome-resolved metagenomics and metaproteomics to investigate a cold-water geyser microbial community enriched in Gracilibacteria across a 12-day time-series. Groundwater was collected and sequentially filtered to fraction CPR and other bacteria. Based on 725 Gbps of metagenomic data, 1129 different ribosomal protein S3 marker genes, and 751 high-quality genomes (123 population genomes after dereplication), we identified dominant bacteria belonging to Gallionellales and Gracilibacteria along with keystone microbes, which were low in genomic abundance but substantially contributing to proteomic abundance. Seven high-quality Gracilibacteria genomes showed typical limitations, such as limited amino acid or nucleotide synthesis, in their central metabolism but no co-occurrence with potential hosts. The genomes of these Gracilibacteria were encoded for a high number of proteins involved in cell to cell interaction, supporting the previously surmised host-dependent lifestyle, e.g., type IV and type II secretion system subunits, transporters, and features related to cell motility, which were also detected on protein level.

Conclusions: We here identified microbial keystone taxa in a high-CO2 aquifer, and revealed microbial dynamics of Gracilibacteria. Although Gracilibacteria in this ecosystem did not appear to target specific organisms in this ecosystem due to lack of co-occurrence despite enrichment on 0.2-µm filter fraction, we provide proteomic evidence for the complex machinery behind the host-dependent lifestyle of groundwater Gracilibacteria. Video Abstract.

高二氧化碳含水层群落的元蛋白基因组学分析揭示了地下水藻类对依赖于宿主的生活方式的复杂细胞适应。
背景:候选菌门辐射(CPR)细菌约占细菌生物多样性的 25%,其特点是细胞体积小,基因组不完整,没有完整的关键代谢途径,表明其生活方式为共生。格拉西利细菌(BD1-5)是CPR分支的一部分,拥有交替编码的基因组,尚未被培养。格拉西菌的生活方式、时间动态以及在自然生态系统(尤其是地下水)中的活动在很大程度上仍未得到研究。在这里,我们利用德国埃菲尔火山地区冷水间歇泉 Wallender Born 中格拉西利细菌的元蛋白基因组与时间的函数关系,旨在研究格拉西利细菌的原位活动,并根据表达的基因来辨别它们的生活方式:我们将基因组分辨元基因组学和元蛋白质组学结合起来,研究了冷水间歇泉微生物群落在 12 天时间序列中富含的格拉西菌。采集地下水并按顺序过滤,以去除CPR和其他细菌。根据 725 Gbps 的元基因组数据、1129 个不同的核糖体蛋白 S3 标记基因和 751 个高质量基因组(去复制后的 123 个群体基因组),我们确定了属于 Gallionellales 和 Gracilibacteria 的优势细菌以及关键微生物,它们的基因组丰度较低,但对蛋白质组丰度有很大贡献。七个高质量的鹩啼菌基因组显示了其中央代谢的典型局限性,如氨基酸或核苷酸合成有限,但没有与潜在宿主共生。这些格拉西勒氏菌的基因组中编码了大量参与细胞间相互作用的蛋白质,支持之前推测的依赖宿主的生活方式,如IV型和II型分泌系统亚基、转运体以及与细胞运动有关的特征,这些蛋白质也在蛋白质水平上被检测到:我们在此确定了高二氧化碳含水层中的微生物关键类群,并揭示了砾岩菌的微生物动态。尽管0.2微米滤液中富集了鹩啼菌,但由于鹩啼菌没有共同出现,因此该生态系统中的鹩啼菌似乎并不以特定生物为目标,我们为地下水鹩啼菌依赖于宿主的生活方式背后的复杂机制提供了蛋白质组学证据。视频摘要。
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来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
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