Communications Biology volume：跨生物群落微生物网络揭示了功能冗余，并建议通过功能互补减少基因组-动脉网

Communications Biology volume：Cross-biome microbial networks reveal functional redundancy and suggest genome reduction through functional complementarity

Nature 等信源发布 2024-08-24 21:37

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AbstractThe structure of microbial communities arises from a multitude of factors, including the interactions of microorganisms with each other and with the environment. In this work, we sought to disentangle those drivers by performing a cross-study, cross-biome meta-analysis of microbial occurrence data in more than 5000 samples, applying a novel network clustering algorithm aimed to capture conditional taxa co-occurrences.

摘要微生物群落的结构来自多种因素，包括微生物之间以及与环境的相互作用。在这项工作中，我们试图通过对5000多个样本中的微生物发生数据进行交叉研究，跨生物组荟萃分析来解开这些驱动因素，应用一种旨在捕获条件分类群共现的新型网络聚类算法。

We then examined the phylogenetic and functional composition of the resulting clusters, and searched for global patterns of assembly both at the community level and in the presence/absence of individual metabolic pathways.Our analysis highlighted the prevalence of functional redundancy in microbial communities, particularly between taxa that co-occur in more than one environment, pointing to a relationship between functional redundancy and environmental adaptation.

然后，我们检查了所得簇的系统发育和功能组成，并在社区层面和存在/不存在个体代谢途径的情况下搜索了全球组装模式。我们的分析强调了微生物群落中功能冗余的普遍性，特别是在多个环境中共同出现的分类群之间，指出了功能冗余与环境适应之间的关系。

In spite of this, certain pathways were observed in fewer taxa than expected by chance, suggesting the presence of auxotrophy, and presumably cooperation among community members. This hypothetical cooperation may play a role in genome reduction, since we observed a negative relationship between the size of bacterial genomes and the size of the community they belong to.Overall, our results suggest the microbial community assembly is driven by universal principles that operate consistently across different biomes and taxonomic groups..

尽管如此，在偶然的情况下，在较少的分类群中观察到某些途径，这表明存在营养缺陷，并且可能是社区成员之间的合作。这种假设性的合作可能在基因组减少中发挥作用，因为我们观察到细菌基因组的大小与其所属群落的大小之间存在负相关关系。总的来说，我们的结果表明微生物群落的组装是由普遍原理驱动的，这些原理在不同的生物群落和分类学群体中始终如一地起作用。。

IntroductionMicroorganisms are the second most abundant component of the global biomass on Earth1, and the first one in terms of biodiversity2. In addition, they are the only ones capable of performing key ecological functions, including nitrogen fixation, methanogenesis, and all kinds of anaerobic respirations.

。此外，它们是唯一能够执行关键生态功能的生物，包括固氮，产甲烷和各种无氧呼吸。

As such, they play a critical role in driving the essential biogeochemical cycles that sustain life on our planet3. Microorganisms interact among themselves and with the environment, giving rise to emergent community-level properties4,5. These interactions are primary driving forces in microbial ecology, and determine the fate of microbial communities and, by extension, of their constituent microorganisms4.

因此，它们在推动维持我们星球上生命的基本生物地球化学循环中起着至关重要的作用3。微生物之间以及与环境的相互作用，产生了新兴的社区层面的属性4,5。这些相互作用是微生物生态学的主要驱动力，并决定微生物群落的命运，进而决定其组成微生物的命运4。

Therefore, the study of individual microorganisms is often not enough to predict how those very same microorganisms will behave in nature; instead, they have to be considered in the context of the community they live in.Microbial communities are complex and dynamic entities, and their structure arises from the interplay of four key ecological processes: selection, diversification, dispersal and drift6,7.

因此，对单个微生物的研究通常不足以预测这些微生物在自然界中的行为；相反，它们必须在它们所生活的社区的背景下进行考虑。微生物群落是复杂而动态的实体，它们的结构来自四个关键生态过程的相互作用：选择，多样化，扩散和漂移6,7。

Among them, selection (i.e., the existence of fitness differences between individuals) is a primary force shaping microbial community assembly4,7,8. Natural selection counteracts random fluctuations and acts over short timescales, which makes it experimentally tractable9,10,11. This has led to an increasing interest in synthetic microbial ecology as a tool to generate and test hypotheses regarding community assembly processes (reviewed in ref.

其中，选择（即个体之间适应性差异的存在）是形成微生物群落组装的主要力量4,7,8。自然选择抵消了随机波动，并在短时间内起作用，这使得它在实验上易于处理9,10,11。这导致人们越来越关注合成微生物生态学，将其作为产生和检验有关群落组装过程假设的工具（参见参考文献）。

12). However, the simplicity inherent to synthetic microbial communities, while facilitating their precise characterization, might also limit their usefulness as proxies of natural microbial communities13,14.A complemen.

12）。然而，合成微生物群落固有的简单性，在促进其精确表征的同时，也可能限制其作为天然微生物群落替代物的有用性13,14。一个完整的例子。

For each of the ten environments included in this study:

对于本研究中包括的十个环境中的每一个：

11.

Compute aggregation Z-scores between pairs of taxa i, j in samples a from the binary presence/absence matrix Xia and the probability matrix πia as described in Supplementary Note 1.

如补充说明1所述，从二元存在/不存在矩阵Xia和概率矩阵πia计算样本a中分类群i，j对之间的聚集Z分数。

12.

Create 100 independent networks (in order to minimize path dependency during the clustering process) applying the following clustering procedure. We will refer generically to “nodes” for both individual taxa (e.g. elements at the beginning of the algorithm) and assemblages (taxa clustered together):.

应用以下聚类过程创建100个独立的网络（以最大程度地减少聚类过程中的路径依赖性）。对于单个分类群（例如算法开始时的元素）和集合（聚集在一起的分类群），我们通常会提到“节点”：。

121.

While there are significantly associated pairs of nodes appearing together in more than 5 samples:

虽然在5个以上的样本中同时出现了显着相关的节点对：

1211.

Select one significantly associated pair i,j at random, weighted by its aggregation Z-score so that pairs with higher aggregation scores are more likely to be selected.

随机选择一个显着相关的对i，j，通过其聚集Z分数加权，以便更有可能选择聚集分数较高的对。

1212.

Create a new node k that represents the aggregation of the selected pair of nodes i,j in the samples in which they appear together, with \({X}_{{ka}}={X}_{{ia}}\cdot {X}_{{ja}}\) and \({\pi }_{{ka}}={\pi }_{{ia}}\cdot {\pi }_{{ja}}\).

\({X}_{{ka}}={X}_{{ia}}\c点{X}_{{{ja}}和\（{\pi}{{ka}}={\pi}{{{ia}}\cdot{\pi}}{{ja}}\）。

1213.

Create the links i → k and j → k.

创建链接i→k和j→k。

1214.

Replace the values for i and j in the presence/absence matrix and in the probability matrix, so that they represent the presence of i and j in the samples in which they do not appear together, with \({X}_{i^{\prime} a}={X}_{{ia}}\cdot (1-{X}_{{ja}})\), \({\pi }_{i^{\prime} a}={\pi }_{{ia}}\cdot (1-{\pi }_{{ja}})\), \({X}_{j{\prime} a}={X}_{{ja}}\cdot (1-{X}_{{ia}})\) and \({\pi }_{j^{\prime} a}={\pi }_{{ja}}\cdot (1-{\pi }_{{ia}})\)..

替换存在/不存在矩阵和概率矩阵中i和j的值，以便它们表示i和j在不同时出现的样本中的存在，以及\({X}_{i ^{\素数}a}={X}_{{ia}}\cdot（1-{X}_{{{ja}}）\），\（{\pi}u{i^{\prime}a}={\pi}u{{ia}}\cdot（1-{\pi}u{{ja}）\）\({X}_{j{\素数}a}={X}_{{{ja}}\cdot（1-{X}_{{{ia}}）和\（{pi}{uj^{\ prime}a}={\ pi}{{{ja}}\ cdot（1-{\ pi}}{{{{ia}}）\）。。

1215.

Recalculate the aggregation Z-scores from the new X and π matrices.

从新的X和π矩阵重新计算聚合Z分数。

Combine the 1000 independent networks (100 networks from each of the 10 environments) into a single network as follows:.

将1000个独立网络（10个环境中的每一个都有100个网络）组合成一个网络，如下所示：。

21.

The combined network contains all the nodes present in the individual networks. Nodes containing the same taxa in the individual networks are collapsed into a single node in the combined network.

组合网络包含各个网络中存在的所有节点。在单个网络中包含相同分类群的节点被折叠成组合网络中的单个节点。

22.

All incoming and outgoing edges present in the individual networks are added to the collapsed nodes in the combined network.

单个网络中存在的所有传入和传出边缘都将添加到组合网络中的折叠节点中。

23.

For each node and edge, we define its support value as the number of individual networks in which that node or edge was observed. Nodes and edges with a support value smaller than 10 are discarded.

对于每个节点和边缘，我们将其支持值定义为观察到该节点或边缘的单个网络的数量。支持值小于10的节点和边将被丢弃。

24.

Nodes are annotated based on the source environment of the individual networks in which they were found.

节点根据发现它们的各个网络的源环境进行注释。

Environmental and bibliographic annotation of assemblagesFor each sample, the microDB database contains its isolation source, as originally found in the NCBI GenBank database, as well as the Pubmed ID (PMID) of any published work related to it. We annotated each assemblage representing a significant aggregation of two or more genera with the isolation sources and related PMIDs of the samples in which the genera appeared together.Functional annotation of assemblages and intra-assemblage functional redundancyWe used the MetaCyc database version 1927 to download the predicted reactomes for all the sequenced genomes from the genera included in our network (Supplementary Data 3).

集合的环境和书目注释对于每个样本，microDB数据库包含最初在NCBI GenBank数据库中找到的隔离源，以及与之相关的任何已发表作品的Pubmed ID（PMID）。我们注释了每个集合，代表两个或多个属的显着聚集，以及这些属一起出现的样本的隔离源和相关PMID。集合的功能注释和集合内功能冗余我们使用MetaCyc数据库版本1927从我们网络中包含的属中下载所有测序基因组的预测反应组（补充数据3）。

For each genome, we predicted its metabolic pathways from its reactome using an in-house implementation of the PathoLogic algorithm as described in26. As a deviation from the original algorithm, we did not add a more lenient prediction rule for energy metabolism pathways, as we found out that doing so would result in false positive predictions (e.g.

对于每个基因组，我们使用26中描述的病理算法的内部实现，从其反应组预测其代谢途径。作为与原始算法的偏差，我们没有为能量代谢途径添加更宽松的预测规则，因为我们发现这样做会导致假阳性预测（例如。

sulfate respiration would be predicted for Escherichia). The fraction of genomes from each genus that contain each pathway is reported in Supplementary Data 4. We considered that a pathway is present in a genus if it is predicted in all of the complete genomes from that genus (i.e. the pathway belongs to the core genome of the genus).

硫酸盐呼吸将被预测为埃希氏菌）。。如果在该属的所有完整基因组中都预测了一条途径，我们认为该途径存在于该属中（即该途径属于该属的核心基因组）。

In Supplementary Note 2, we show how genus-level core genomes are reasonably similar regardless of whether they are calculated using reference genomes or genomes from environmental strains, and that as such our functional inference approach provides a good approximation to the core core genomes of the environmental strains that were originally present in our samples.

在补充说明2中，我们展示了属级核心基因组是如何合理相似的，无论它们是使用参考基因组还是使用环境菌株的基因组计算的，因此我们的功能推断方法提供了一个很好的近似于核心核心基因组的环境菌株最初存在于我们的样本中。

We then defined the pathways present in an assemblage {R}.

。

1000 random assemblages with the same number of genera as the real assemblage.

1000个随机组合，其属数与真实组合相同。

b。

100 environmentally-equivalent random assemblages with the same number of genera as the real assemblage, such that their genera came from the same environmental subtype (i.e. the finest environmental classification available in the microDB database, see ref. 24).

100个具有与实际组合相同属数的环境等效随机组合，使得它们的属来自相同的环境亚型（即microDB数据库中可用的最佳环境分类，参见参考文献24）。

c。

100 environmentally/phylogenetically-equivalent random assemblages with the same number of genera as the real assemblage, such that their genera came from the same environmental subtype and the average pairwise phylogenetic distances in the random assemblages differed by 0.05 substitutions per position or less from the average pairwise phylogenetic distance of the original assemblage.

100个环境/系统发育等效的随机组合，其属数与真实组合相同，因此它们的属来自相同的环境亚型，并且随机组合中的平均成对系统发育距离与每个位置的平均成对系统发育距离相差0.05个取代或更少原始组合的平均成对系统发育距离。

This was done in order to assess whether functional redundancy could be explained by phylogenetic similarity and source environment alone..

这样做是为了评估功能冗余是否可以仅通过系统发育相似性和源环境来解释。。

d。

100 environmentally/genome size-equivalent random assemblages with the same number of genera as the real assemblage, such that their genera came from the same environmental subtype and the average number of pathways per genus differed by 20% of less from the average number of pathways in the original assemblage..

100个环境/基因组大小相当的随机组合，其属数与真实组合相同，因此它们的属来自相同的环境亚型，每个属的平均途径数与原始组合中的平均途径数相差20%。。

We assessed significant differences between different types or assemblages with the Mann-Whitney U test. For each metric (average intra-assemblage functional distance, average intra-assemblage phylogenetic distance and average number of pathways in the assemblage members) and assemblage size, the resulting p-values were corrected for multiple testing using the Benjamini-Hochberg method73.Detection of redundant and specific pathways in the assemblages of our networkThe procedure described above provided us with a per-assembly estimate of functional redundancy, but we were also interested in assessing functional redundancy on a per-pathway basis.

我们使用Mann-Whitney U检验评估了不同类型或组合之间的显着差异。对于每个度量（平均集合内功能距离，平均集合内系统发育距离和集合成员中路径的平均数量）和集合大小，使用Benjamini-Hochberg方法73对产生的p值进行多重测试校正。检测我们网络集合中的冗余和特定路径上述过程为我们提供了功能冗余的每个集合估计，但我们也有兴趣在每个路径的基础上评估功能冗余。

For this, we first selected a subset of the network connected by highly supported (support > 70) edges. We then selected the terminal assemblages with no outgoing edges to larger assemblages, which represent the sink nodes of our clustering algorithm. For each of these assemblages, we then generated 1,000 phylogenetically and environmentally equivalent random assemblages (see previous section).

为此，我们首先选择了由高度支持（支持>70）边连接的网络子集。然后，我们将没有传出边缘的终端集合选择为较大的集合，这些集合代表了我们聚类算法的汇聚节点。然后，对于这些组合中的每一个，我们生成了1000个系统发育和环境等效的随机组合（请参见上一节）。

In order to obtain a higher number of valid random assemblages, we increased the maximum difference in phylogenetic distances from 0.01 to 0.1 substitutions per position. Then, for each metabolic pathway, we compared its prevalence in the real assemblage with its prevalence in the random assemblages and classified it into one three categories:.

为了获得更多的有效随机组合，我们将系统发育距离的最大差异从每个位置的0.01个替换增加到0.1个替换。然后，对于每个代谢途径，我们将其在真实组合中的患病率与在随机组合中的患病率进行了比较，并将其分为三类：。

Redundant, if it appeared in at least two members of the real assemblage, and its prevalence was higher than its prevalence in 95% of the random assemblages.

如果它出现在真实组合的至少两个成员中，并且其患病率高于其在95%的随机组合中的患病率，则是多余的。

Specific, if appeared in the real assemblage, but its prevalence was lower than its prevalence in 95% of the random assemblages.

具体而言，if出现在真实组合中，但其患病率低于95%的随机组合中的患病率。

Missing, if it was missing from the real assemblage, but present in 95% of the random assemblages.

缺失，如果它在真实组合中缺失，但在95%的随机组合中存在。

Finally, for each metabolic pathway, we computed the fraction of auxotrophs in a given assembly as 1-P/S where P is its prevalence in the assemblage, and S is the size of the assemblage.Reporting summaryFurther information on research design is available in the Nature Portfolio Reporting Summary linked to this article..

最后，对于每个代谢途径，我们将给定装配中营养缺陷型的比例计算为1-P/S，其中P是其在装配中的流行程度，S是装配的大小。报告摘要有关研究设计的更多信息，请参阅本文链接的Nature Portfolio Reporting Summary。。

Data availability

数据可用性

The data used in this work are publicly available at https://github.com/fpusan/cross-biome-microbial-networks with https://doi.org/10.5281/zenodo.12770646. A SQL dump of the database used in this work can be found at https://github.com/fpusan/cross-biome-microbial-networks/tree/main/00-algorithm.

这项工作中使用的数据可在https://github.com/fpusan/cross-biome-microbial-networks与https://doi.org/10.5281/zenodo.12770646.这项工作中使用的数据库的SQL转储可以在https://github.com/fpusan/cross-biome-microbial-networks/tree/main/00-algorithm.

Code availability

代码可用性

The code used in this work is publicly available at https://github.com/fpusan/cross-biome-microbial-networks with https://doi.org/10.5281/zenodo.12770646.

https://github.com/fpusan/cross-biome-microbial-networks与https://doi.org/10.5281/zenodo.12770646.

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Download referencesAcknowledgementsAP-G was supported by the Simons Collaboration: Principles of Microbial Ecosystems (PriME), award number 542381, a Ramón y Cajal Fellowship from the Spanish Ministry of Science and Innovation (RyC2021-032424-I), by CSIC intramural project 20232AT031 and by grant PID2022-139900NA-I00 (AEI/10.13039/501100011033/ FEDER, UE).

下载参考文献SAP-G得到了西蒙斯合作：微生物生态系统原理（PriME）的支持，奖项编号542381，西班牙科学与创新部（RyC2021-032424-I）的Ramón y Cajal奖学金，CSIC校内项目20232AT031和grant PID2022-139900NA-I00（AEI/10.13039/501100011033/FEDER，UE）的支持。

UB was supported through the grant PID2019-109041GB-C22/10.13039/501100011033 of the Spanish Agency of Research (AEI). Research at the CBMSO is facilitated by the Fundación Ramón Areces. FP-S was funded by grant CTM2016-80095-C2-1-R / NOVAMAR from the Spanish Ministerio de Economía y Competitividad, the Marie Skłodowska-Curie grant agreement No 892961 from the European Union’s Horizon 2020 research and innovation programme and grant 2022-04801 from the Swedish Research Council..

UB得到了西班牙研究机构（AEI）的资助PID2019-109041GB-C22/10.13039/501100011033的支持。。FP-S由西班牙经济与竞争部授予的CTM2016-80095-C2-1-R/NOVAMAR资助，欧盟地平线2020研究与创新计划授予的第892961号Marie Skłodowska-Curie资助协议以及瑞典研究理事会授予的2022-04801资助。。

This article first appeared online as a preprint with https://doi.org/10.1101/2022.09.11.507163.FundingOpen access funding provided by Swedish University of Agricultural Sciences.Author informationAuthors and AffiliationsSystems Biology Department, Centro Nacional de Biotecnología (CSIC), C/ Darwin 3, Campus de Cantoblanco, 28049, Madrid, SpainFernando Puente-Sánchez, Alberto Pascual-García, Carlos Pedrós-Alió & Javier TamamesDepartment of Aquatic Sciences and Assessment, Swedish University for Agricultural Sciences (SLU), Lennart Hjelms väg 9, 756 51, Uppsala, SwedenFernando Puente-SánchezComputational Biology and Bioinformatics, Centro de Biología Molecular Severo Ochoa (Universidad Autónoma de Madrid - CSIC), C/ Nicolás Cabrera 1, Campus de Cantoblanco, 28049, Madrid, SpainUgo BastollaAuthorsFernando Puente-SánchezView author publicationsYou can also search for this author in.

本文首次在网上以预印本的形式出现https://doi.org/10.1101/2022.09.11.507163.FundingOpen瑞典农业科学大学提供的获取资金。作者信息作者和附属机构系统生物学系，国家生物技术中心（CSIC），C/Darwin 3，Cantoblanco校区，28049，马德里，Spafernando Puente-Sánchez，Alberto Pascual García，Carlos PedróS-Alió&Javier Tamames瑞典农业科学大学（SLU）水生科学与评估系，Lennart Hjelms väg 9756; g 951，Uppsala，SwedenFernando Puente-SánchezComputational Biología分子Severo Ochoa（马德里自治大学-CSIC），C/NicoláS Cabrera 1，Campus de Cantoblanco，28049，Madrid，SpainUgo BastollaAuthorsFernando Puente-SánchezView作者出版物你也可以在中搜索这位作者。

PubMed Google ScholarAlberto Pascual-GarcíaView author publicationsYou can also search for this author in

PubMed Google ScholarAlberto Pascual GarcíaView作者出版物您也可以在

PubMed Google ScholarUgo BastollaView author publicationsYou can also search for this author in

PubMed Google ScholarUgo BastollaView作者出版物您也可以在

PubMed Google ScholarCarlos Pedrós-AlióView author publicationsYou can also search for this author in

PubMed Google ScholarCarlos Pedrós-AlióView作者出版物您也可以在

PubMed Google ScholarJavier TamamesView author publicationsYou can also search for this author in

PubMed Google ScholarJavier TamamesView作者出版物您也可以在

PubMed Google ScholarContributionsFP-S: Conceptualization, Methodology, Software, Validation, Formal Analysis, Investigation, Writing – Original Draft, Visualization; AP-G: Conceptualization, Methodology, Software, Validation, Writing - Review & Editing; UB: Conceptualization, Methodology, Writing - Review & Editing; CP-A: Writing - Review & Editing, Supervision, Funding acquisition; JT: Conceptualization, Resources, Data Curation, Writing - Review & Editing, Supervision, Funding acquisition, Project administration.Corresponding authorCorrespondence to.

PubMed谷歌学术贡献SFP-S：概念化，方法论，软件，验证，形式分析，调查，写作-原稿，可视化；AP-G：概念化，方法论，软件，验证，写作-评论和编辑；UB：概念化，方法论，写作-评论和编辑；CP-A：写作-评论和编辑，监督，资金获取；JT：概念化，资源，数据管理，写作-评论和编辑，监督，资金获取，项目管理。对应作者对应。

Fernando Puente-Sánchez.Ethics declarations

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Communications Biology thanks Christian Diener, Luke Thompson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Anna Heintz-Buschart and Tobias Goris. [A peer review file is available.]

《传播生物学》感谢克里斯蒂安·迪纳（Christian Diener）、卢克·汤普森（Luke Thompson）和另一位匿名审稿人对这项工作的同行评审所做的贡献。主要处理编辑：安娜·海因茨·布沙特（Anna Heintz Buschart）和托拜厄斯·戈利斯（Tobias Goris）。[可获得同行评审文件。]

Additional informationPublisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary informationPeer Review FileSupplementary InformationDescription of Additional Supplementary FilesSupplementary Data 1Supplementary Data 2Supplementary Data 3Supplementary Data 4Reporting SummaryRights and permissions.

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Reprints and permissionsAbout this articleCite this articlePuente-Sánchez, F., Pascual-García, A., Bastolla, U. et al. Cross-biome microbial networks reveal functional redundancy and suggest genome reduction through functional complementarity.

转载和许可本文引用本文Puente-Sánchez，F.，Pascual-García，a.，Bastolla，U。等人。跨生物群落微生物网络揭示了功能冗余，并建议通过功能互补减少基因组。

Commun Biol 7, 1046 (2024). https://doi.org/10.1038/s42003-024-06616-5Download citationReceived: 26 June 2023Accepted: 23 July 2024Published: 24 August 2024DOI: https://doi.org/10.1038/s42003-024-06616-5Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

Commun Biol 71046（2024）。https://doi.org/10.1038/s42003-024-06616-5Download引文接收日期：2023年6月26日接收日期：2024年7月23日发布日期：2024年8月24日OI：https://doi.org/10.1038/s42003-024-06616-5Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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Subjects

Community ecologyEcological networksEcosystem ecologyMicrobial ecologyMicrobiome

社区生态网络生态系统生态微生物生态群落

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