Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota
Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota
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DOI：
10.1128/msystems.00288-19
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发表时间：
2019-07
期刊：
影响因子：
6.4
通讯作者：
Sha Zhang;Weizhi Song;B. Wemheuer;J. Reveillaud;N. Webster;T. Thomas
中科院分区：
文献类型：
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作者：
Sha Zhang;Weizhi Song;B. Wemheuer;J. Reveillaud;N. Webster;T. Thomas
海绵是了解后生动物与微生物共生体共生相互作用演化的重要生态模型。Thaumarchaeota通常在海绵中发现，但它们对宿主相关生活方式的潜在适应在很大程度上是未知的。在这里，我们提出了三种新的海绵相关的thaumarchaeal物种，并比较其基因组和预测的功能特征与密切相关的自由生活的同行。我们发现不同程度的专业化，这些thaumarchaeal物种的海绵环境，反映在他们的主机分布和预测的分子和代谢特性。我们的研究结果表明，Thaumarchaeota可能已经达到了不同阶段的进化适应，在他们的共生海绵。摘要Thaumarchaeota经常被报道与海绵（多孔动物门）有关;然而，很少有人知道它们与自由生活的Thaumarchaeal对应物的区别特征。在这项研究中，thaumarchaeal宏基因组组装基因组（MAG）的数据集来自海绵Hexadella acetatifera，Hexadella cf.和扇叶柱花草（Stylissa flabelliformis）。系统发育和分类学分析表明，这3个嗜盐古菌代表了Nitrosopumilus属中的2个新种和1个新属，我们建议将其命名为“Aphrodatus UNitrosopumilus hexadellus”、“Aphrodatus UNitrosopumilus acetatiferus”和“Aphrodatus UCenporiarchaeum stylissum”（上标U表示该分类单元未培养）。将这些基因组与海绵地球微生物组计划的数据进行比较，发现“Ca. UCenporiarchaeum stylissum”仅在海绵中检测到，因此可以被归类为专家，而“Ca. Unitrosopumilus acidtiferus”和“Ca.在海绵全生生物外也发现了“六角单亚硝化菌”，并可能过着多面手的生活方式。海绵相关的MAG的基因组的自由生活Thaumarchaeota的比较显示的签名，表明海绵相关的生活方式的功能特征，这些功能与营养运输和代谢，限制修饰，防御机制，和主机的相互作用。每个物种都表现出不同的功能特征，这表明它们已经达到了不同的进化适应阶段和/或在其海绵宿主中占据不同的生态位。因此，我们的研究为海绵和它们的thaumarchaeal共生体之间的共生关系提供了新的进化和生态学见解。重要性海绵代表生态学上重要的模型，以了解共生相互作用的后生动物与微生物共生体的演变。Thaumarchaeota通常在海绵中发现，但它们对宿主相关生活方式的潜在适应在很大程度上是未知的。在这里，我们提出了三种新的海绵相关的thaumarchaeal物种，并比较其基因组和预测的功能特征与密切相关的自由生活的同行。我们发现不同程度的专业化，这些thaumarchaeal物种的海绵环境，反映在他们的主机分布和预测的分子和代谢特性。我们的研究结果表明，Thaumarchaeota可能已经达到了不同阶段的进化适应，在他们的共生海绵。
Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges. ABSTRACT Thaumarchaeota are frequently reported to associate with marine sponges (phylum Porifera); however, little is known about the features that distinguish them from their free-living thaumarchaeal counterparts. In this study, thaumarchaeal metagenome-assembled genomes (MAGs) were reconstructed from metagenomic data sets derived from the marine sponges Hexadella detritifera, Hexadella cf. detritifera, and Stylissa flabelliformis. Phylogenetic and taxonomic analyses revealed that the three thaumarchaeal MAGs represent two new species within the genus Nitrosopumilus and one novel genus, for which we propose the names “Candidatus UNitrosopumilus hexadellus,” “Candidatus UNitrosopumilus detritiferus,” and “Candidatus UCenporiarchaeum stylissum” (the U superscript indicates that the taxon is uncultured). Comparison of these genomes to data from the Sponge Earth Microbiome Project revealed that “Ca. UCenporiarchaeum stylissum” has been exclusively detected in sponges and can hence be classified as a specialist, while “Ca. UNitrosopumilus detritiferus” and “Ca. UNitrosopumilus hexadellus” are also detected outside the sponge holobiont and likely lead a generalist lifestyle. Comparison of the sponge-associated MAGs to genomes of free-living Thaumarchaeota revealed signatures that indicate functional features of a sponge-associated lifestyle, and these features were related to nutrient transport and metabolism, restriction-modification, defense mechanisms, and host interactions. Each species exhibited distinct functional traits, suggesting that they have reached different stages of evolutionary adaptation and/or occupy distinct ecological niches within their sponge hosts. Our study therefore offers new evolutionary and ecological insights into the symbiosis between sponges and their thaumarchaeal symbionts. IMPORTANCE Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges.