Microbial occurrence and symbiont detection in a global sample of lichen metagenomes.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences
PLoS Biology Pub Date : 2024-11-07 eCollection Date: 2024-11-01 DOI:10.1371/journal.pbio.3002862
Gulnara Tagirdzhanova, Paul Saary, Ellen S Cameron, Carmen C G Allen, Arkadiy I Garber, David Díaz Escandón, Andrew T Cook, Spencer Goyette, Veera Tuovinen Nogerius, Alfredo Passo, Helmut Mayrhofer, Håkon Holien, Tor Tønsberg, Lisa Y Stein, Robert D Finn, Toby Spribille
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引用次数: 0

Abstract

In lichen research, metagenomes are increasingly being used for evaluating symbiont composition and metabolic potential, but the overall content and limitations of these metagenomes have not been assessed. We reassembled over 400 publicly available metagenomes, generated metagenome-assembled genomes (MAGs), constructed phylogenomic trees, and mapped MAG occurrence and frequency across the data set. Ninety-seven percent of the 1,000 recovered MAGs were bacterial or the fungal symbiont that provides most cellular mass. Our mapping of recovered MAGs provides the most detailed survey to date of bacteria in lichens and shows that 4 family-level lineages from 2 phyla accounted for as many bacterial occurrences in lichens as all other 71 families from 16 phyla combined. Annotation of highly complete bacterial, fungal, and algal MAGs reveals functional profiles that suggest interdigitated vitamin prototrophies and auxotrophies, with most lichen fungi auxotrophic for biotin, most bacteria auxotrophic for thiamine and the few annotated algae with partial or complete pathways for both, suggesting a novel dimension of microbial cross-feeding in lichen symbioses. Contrary to longstanding hypotheses, we found no annotations consistent with nitrogen fixation in bacteria other than known cyanobacterial symbionts. Core lichen symbionts such as algae were recovered as MAGs in only a fraction of the lichen symbioses in which they are known to occur. However, the presence of these and other microbes could be detected at high frequency using small subunit rRNA analysis, including in many lichens in which they are not otherwise recognized to occur. The rate of MAG recovery correlates with sequencing depth, but is almost certainly influenced by biological attributes of organisms that affect the likelihood of DNA extraction, sequencing and successful assembly, including cellular abundance, ploidy and strain co-occurrence. Our results suggest that, though metagenomes are a powerful tool for surveying microbial occurrence, they are of limited use in assessing absence, and their interpretation should be guided by an awareness of the interacting effects of microbial community complexity and sequencing depth.

地衣元基因组全球样本中的微生物出现和共生体检测。
在地衣研究中,元基因组越来越多地被用于评估共生体的组成和代谢潜力,但这些元基因组的总体内容和局限性尚未得到评估。我们重新组装了400多个公开的元基因组,生成了元基因组组装基因组(MAGs),构建了系统发生树,并绘制了整个数据集的MAG发生率和频率图。在回收的 1000 个 MAG 中,97% 是细菌或真菌共生体,它们提供了大部分的细胞质量。我们对回收的 MAGs 的绘图提供了迄今为止对地衣中细菌的最详细调查,并显示来自 2 个植物门的 4 个科级世系在地衣中出现的细菌数量相当于来自 16 个植物门的所有其他 71 个科的总和。对高度完整的细菌、真菌和藻类 MAGs 的注释揭示了功能特征,表明维生素原养和辅养相互交织,大多数地衣真菌辅养生物素,大多数细菌辅养硫胺素,少数注释的藻类对两者都有部分或完整的途径,这表明地衣共生中微生物交叉觅食的一个新层面。与长期以来的假设相反,除了已知的蓝藻共生体外,我们没有发现与细菌固氮作用一致的注释。藻类等核心地衣共生体只在一小部分已知的地衣共生体中作为 MAGs 出现。然而,通过小亚基 rRNA 分析,可以高频率地检测到这些微生物和其他微生物的存在,包括在许多地衣中,而这些微生物并没有以其他方式被确认存在。MAG 的回收率与测序深度有关,但几乎可以肯定的是受到生物体生物属性的影响,这些生物属性会影响 DNA 提取、测序和成功组装的可能性,包括细胞丰度、倍性和菌株共存。我们的研究结果表明,虽然元基因组是调查微生物出现情况的有力工具,但在评估缺失情况方面作用有限,在解释元基因组时应注意微生物群落复杂性和测序深度的相互作用。
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来源期刊
PLoS Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
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