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

By Seth R. Bordenstein, K. Theis. PLoS Biology, 2015

1,071 citations recorded by the source corpus.

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.

Subfields: Ecology, Evolution, Behavior and Systematics, Plant Science

View Paper: https://www.semanticscholar.org/paper/4c07e7e5781ff2a7e1501274053521e33a6c6344

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Citations in the corpus

It’s the song, not the singer: an exploration of holobiosis and evolutionary theory (2017, background): “…a gene in the nuclear genome to a microbe in the microbiome… Evolution for both genes and symbionts is fundamentally a change in population frequency over successive generations, i.e., the fraction of holobionts carrying that particular nuclear allele or microbe (Bordenstein and Theis 2015, 3).”
Holobionts and the ecology of organisms: Multi-species communities or integrated individuals? (2016, background): “Thus, variation in the hologenome can lead to variation in phenotypes upon which natural selection or genetic drift can operate” (Bordenstein and Theis 2015).”
The Central Nervous System and the Gut Microbiome (2016, background): “Moreover, infants are exposed to vertical acquisitions of novel microorganisms through intimate interaction with parents and siblings, as well as exposure to new environments (Bäckhed et al., 2015; Bordenstein and Theis, 2015; Rosenberg and Zilber-Rosenberg, 2016).”
Gut bacteria of field-collected larvae of Spodoptera frugiperda undergo selection and are more diverse and active in metabolizing multiple insecticides than laboratory-selected resistant strains (2020, background): “…of the host genome and the genomes of the associated microbiota (hologenome) (Zilber-Rosenberg and Rosenberg 2008; Rosenberg and Zilber-Rosenberg 2018), which allows the maintenance of complex phenotypes and acts as a source of variability and genetic information (Bordenstein and Theis 2015).”
The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota (2017, background): “ecosystem under selection to minimize conflict between individual members (22).”
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration (2017, background): “The reality is that we have co-evolved, and we are fundamentally dependent upon our colonisers for survival, as of course are they on us (Bordenstein & Theis, 2015).”
Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution (2018, background): “The hologenome concept of evolution has garnered support from many biologists (e.g., Fraune and Bosch 2010; Gilbert et al. 2012; Bordenstein and Theis 2015).”
Stress & the gut-brain axis: Regulation by the microbiome (2017, neutral): “Microbiota and their host organisms co-evolved and are mutually co-dependent for survival, and mammals have never existed without microbes, except in laboratory situations (Bordenstein and Theis, 2015).”
Microbial “gardening” by a seaweed holobiont: Surface metabolites attract protective and deter pathogenic epibacterial settlement (2019, background): “…gut microbiome is very well known to influence the health and nutritional status of its host (Flint, Scott, Louis, & Duncan, 2012; Hooper, Midtvedt, & Gordon, 2002), ultimately forming a metaorganism or holobiont that consists of the host and associated microbiomes (Bordenstein & Theis, 2015).”
Root Exudation: The Ecological Driver of Hydrocarbon Rhizoremediation (2016, background): “The microbial portion of the plant holobiont can be seen as a “facilitator component” that provides additional genes to the host and allows it to adjust to environmental conditions [90,92].”