Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.

Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.
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DOI:
10.1371/journal.pbio.1002226
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发表时间:
2015-08
期刊:
影响因子:
9.8
通讯作者:
Theis KR
Theis KR
中科院分区:
生物学1区
文献类型:
--
作者:
Bordenstein SR;Theis KR

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关于微生物普遍性和多样性的开创性研究,如今正促使生命科学对曾经看似不可撼动的基础理论进行升级。要充分理解该领域正在经历的变革,人们必须根据当前的进展(这些进展使人们对微生物学的核心重要性有了新的认识),将达尔文、孟德尔所处的时代以及现代综合进化论的基本原理纳入考量。动植物不再被视为自主的实体,而是被看作由宿主及其相关微生物组成的生物分子网络,即“共生功能体”。如此一来,它们的集体基因组形成了一个“全基因组”,而没有考虑这些基因组间关联的动植物生物学模型是不完整的。在此,我们将这些概念融入生物学的历史和当代视角,并总结出一个可预测且可反驳的框架用于对其进行评估。具体而言,我们提出了十条原则,阐明并补充了这些概念的内涵与外延,解释了它们如何既支持又拓展了生命科学中的现有理论,并讨论了它们对动物学和植物学多方面研究方法的潜在影响。我们预计,本文所提供的基于概念和证据的基础,将为以假设为导向、经实验验证的共生功能体及其全基因组研究提供路线图,从而推动生物学各分支学科的持续融合。在共生微生物被认为对动植物生物学的各个方面都至关重要的当下,共生功能体和全基因组概念提供了一种对生物复杂性的整体视角,这与生物学普遍的还原论方法是一致的。 本文阐述了十条原则,这些原则推动了宿主相关微生物组进化和生态学的统一理论。
Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable. To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology. Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., "holobionts." As such, their collective genomes forge a "hologenome," and models of animal and plant biology that do not account for these intergenomic associations are incomplete. Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation. Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology's subdisciplines. At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology. This Essay lays out ten principles that advance a unified theory of the evolution and ecology of host-associated microbiomes.