Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host

Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host
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DOI:
10.1073/pnas.1902538116
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发表时间:
2019-06
期刊:
Proceedings of the National Academy of Sciences
影响因子:
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通讯作者:
T. Nakayama;M. Nomura;Y. Takano;Goro Tanifuji;Kogiku Shiba;K. Inaba;Y. Inagaki;M. Kawata
T. Nakayama;M. Nomura;Y. Takano;Goro Tanifuji;Kogiku Shiba;K. Inaba;Y. Inagaki;M. Kawata
中科院分区:
其他
文献类型:
--
作者:
T. Nakayama;M. Nomura;Y. Takano;Goro Tanifuji;Kogiku Shiba;K. Inaba;Y. Inagaki;M. Kawata

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意义 蓝藻是海洋微生物生态学的重要组成部分,因此其生物多样性已被广泛研究。在这里,通过全基因组测序,我们发现与单细胞真核生物(OmCyn)共生的海洋蓝藻代表了生态上重要的蓝藻群中先前未被描述的谱系。我们的宏基因组分析表明,蓝藻 OmCyn 在全球海洋中繁衍生息,进一步表明存在其他神秘的蓝藻谱系,这些谱系因其共生生活方式而被忽视。通过与自由生活的亲属的基因组进行比较,OmCyn 基因组被证明具有还原性,这显然是由于与宿主的密切联系所致。总之,我们的结果扩展了目前对蓝藻生物学和海洋微生物生态学的理解。蓝藻是海洋初级生产最重要的贡献者之一,并在广泛的海洋生境中生存。主要基于自由生活的蓝藻物种的数据,人们做出了大量努力来了解它们的生态特征、多样性和进化。此外,共生已成为海洋微生物的一种重要生活方式,并且对蓝藻与单细胞真核生物共生关系的了解不断增加,表明它们对于理解全球海洋生态系统具有重要意义。然而,这些蓝细菌的详细特征仍然很少被描述。为了更好地了解共生中的海洋蓝藻,我们对从远洋甲藻细胞中收集的蓝藻基因组进行了测序,已知该藻类在专门的室内拥有蓝藻共生体。使用基因组序列进行的系统发育分析表明,蓝藻代表了广泛研究的、具有重要生态意义的海洋蓝藻群体中一个未被描述的谱系。宏基因组分析表明,这种蓝藻谱系在全球范围内分布,并与其宿主甲藻严格共存,这表明密切的共生关系使蓝藻逃脱了之前的宏基因组研究。此外,与相关物种的蛋白质库的比较分析表明,该谱系独立地经历了还原性基因组进化,其程度与原绿球藻相似,原绿球藻在自由生活的蓝细菌中基因组减少最多。这种隐藏在共生生活方式中的蓝藻谱系的发现,为了解海洋蓝藻的多样性、生态和进化提供了重要的见解,并表明其他未被发现的神秘蓝藻谱系的存在。
Significance Cyanobacteria are an important component of marine microbial ecology, and thus their biodiversity has been extensively studied. Here, through whole-genome sequencing, we discovered that a marine cyanobacterium in a symbiotic association with a unicellular eukaryote (OmCyn) represents a previously under-described lineage within an ecologically important cyanobacterial group. Our metagenomic analyses showed that the cyanobacterium OmCyn thrives in global oceans, further suggesting the existence of other cryptic cyanobacterial lineages that have been overlooked because of their symbiotic lifestyle. Via comparison with genomes of free-living relatives, the OmCyn genome was shown to have a reductive nature, which apparently resulted from intimate association with the host. Together, our results expand current understanding of the biology of cyanobacteria and marine microbial ecology. Cyanobacteria are one of the most important contributors to oceanic primary production and survive in a wide range of marine habitats. Much effort has been made to understand their ecological features, diversity, and evolution, based mainly on data from free-living cyanobacterial species. In addition, symbiosis has emerged as an important lifestyle of oceanic microbes and increasing knowledge of cyanobacteria in symbiotic relationships with unicellular eukaryotes suggests their significance in understanding the global oceanic ecosystem. However, detailed characteristics of these cyanobacteria remain poorly described. To gain better insight into marine cyanobacteria in symbiosis, we sequenced the genome of cyanobacteria collected from a cell of a pelagic dinoflagellate that is known to host cyanobacterial symbionts within a specialized chamber. Phylogenetic analyses using the genome sequence revealed that the cyanobacterium represents an underdescribed lineage within an extensively studied, ecologically important group of marine cyanobacteria. Metagenomic analyses demonstrated that this cyanobacterial lineage is globally distributed and strictly coexists with its host dinoflagellates, suggesting that the intimate symbiotic association allowed the cyanobacteria to escape from previous metagenomic studies. Furthermore, a comparative analysis of the protein repertoire with related species indicated that the lineage has independently undergone reductive genome evolution to a similar extent as Prochlorococcus, which has the most reduced genomes among free-living cyanobacteria. Discovery of this cyanobacterial lineage, hidden by its symbiotic lifestyle, provides crucial insights into the diversity, ecology, and evolution of marine cyanobacteria and suggests the existence of other undiscovered cryptic cyanobacterial lineages.