Holobiont

A holobiont is a multi-species assemblage consisting of a host organism and its associated communities of microorganisms — bacteria, archaea, fungi, viruses. The term was introduced by Adolf Meyer-Abich in 1943, reintroduced by Lynn Margulis in the context of symbiosis theory, and popularized in coral biology by Forest Rohwer and colleagues. It designates not just the host but the entire consortium of organisms that function as an integrated biological unit.

The human holobiont

A revised cell count estimate published by Sender, Fuchs, and Milo in Cell (2016) found that the human body contains roughly equal numbers of human and microbial cells — approximately 30 trillion of each — overturning the earlier claim of a 10:1 microbial-to-human ratio. The human gut alone harbors over 1,000 bacterial species, with the total microbial gene catalog exceeding human gene count by a factor of roughly 150.

Specific microbial contributions to human physiology include:

• Carbohydrate metabolism. Bacteroides thetaiotaomicron encodes over 260 glycoside hydrolases and polysaccharide lyases, enabling it to break down complex plant polysaccharides that human enzymes cannot digest. Without gut bacteria, humans would extract significantly less energy from dietary fiber.
• Immune training. Colonization of the gut by commensal bacteria is required for normal development of the immune system. Germ-free mice — raised without any microbiome — have underdeveloped gut-associated lymphoid tissue, reduced IgA secretion, impaired T-cell maturation, and abnormal ratios of T helper cell subsets.
• Anti-inflammatory regulation. Faecalibacterium prausnitzii, one of the most abundant bacteria in the healthy human colon, produces butyrate and other short-chain fatty acids that suppress inflammatory signaling. Its depletion is associated with Crohn’s disease and ulcerative colitis.
• Neurological function. The gut microbiome influences brain chemistry through the gut-brain axis. Germ-free mice show altered levels of brain-derived neurotrophic factor (BDNF), increased anxiety-like behavior (Diaz Heijtz et al., 2011), and abnormal serotonin metabolism — Yano et al. (2015) showed that germ-free mice have roughly 60% less serotonin in the colon than conventionally colonized mice, and that indigenous spore-forming bacteria (primarily Clostridia) promote serotonin biosynthesis by host enterochromaffin cells. Fecal microbiota transplantation experiments in mice have demonstrated that behavioral traits — including anxiety phenotypes — can be transferred along with the microbiome. In humans, the FDA approved the first microbiota-based therapies for recurrent Clostridioides difficile infection in 2022-2023 (Rebyota, a fecal microbiota product, and Vowst, an oral capsule formulation), marking the transition of microbiome science into clinical therapeutics.

Germ-free studies and biological individuality

The germ-free mouse model demonstrates that the host organism without its microbiome is not the “real” organism minus accessories — it is a biologically different organism. Germ-free mice have underdeveloped intestinal villi, reduced crypt depth, thinner mucus layers, an immature immune system, altered brain chemistry, and different fat storage patterns compared to conventionally raised mice. Reintroduction of specific bacterial species (gnotobiotic colonization) can rescue these defects in a species-specific manner, demonstrating that particular microbes perform particular functions rather than the microbiome acting as an undifferentiated mass.

These findings raise the question of what counts as a biological individual. The boundary between self and non-self in the holobiont is maintained not by exclusion of all foreign organisms but by active immunological management. The mammalian immune system tolerates beneficial symbionts while surveilling for pathogenic shifts — a distinction maintained through pattern recognition receptors (Toll-like receptors, NOD-like receptors) that detect microbial molecular patterns and calibrate the inflammatory response accordingly.

Coral holobionts

Corals are among the best-studied holobionts. The coral animal hosts endosymbiotic dinoflagellate algae (family Symbiodiniaceae, formerly called zooxanthellae) within its gastrodermal cells. These algae photosynthesize and transfer up to 90% of their fixed carbon to the coral host, providing the energy that builds reef structures. The coral in turn provides the algae with shelter, CO2, and inorganic nutrients.

Coral bleaching occurs when environmental stress — primarily elevated water temperature, but also high light, pollution, or disease — causes the breakdown of this symbiosis. The coral expels its Symbiodiniaceae or the algae lose their photosynthetic pigments, leaving the coral tissue transparent and the white calcium carbonate skeleton visible. Without its photosynthetic partners, the coral can survive for weeks to months on heterotrophic feeding, but prolonged bleaching leads to starvation and death. Mass bleaching events driven by marine heat waves have killed large fractions of coral reefs globally, including an estimated 30% of the Great Barrier Reef’s coral during the 2016 event alone.

The coral holobiont also includes a diverse bacterial community, viruses (including phages that regulate bacterial populations), and endolithic algae within the skeleton. Rohwer and colleagues proposed that the entire assemblage — coral animal, Symbiodiniaceae, bacteria, archaea, fungi, and viruses — functions as a unit of selection, a concept they termed the hologenome theory of evolution.

Hologenome theory and its debate

Zilber-Rosenberg and Rosenberg (2008) proposed that natural selection acts on the holobiont as a unit, with the hologenome — the combined genomes of host and all symbionts — as the relevant genetic entity. Under this view, changes in the microbiome composition can be a mechanism of rapid adaptation, faster than host genetic mutation.

This proposal remains debated. Critics (including Moran and Sloan, 2015; Douglas and Werren, 2016) argue that the holobiont is rarely a coherent unit of selection because the evolutionary interests of host and microbes frequently conflict, microbiome composition is highly variable between individuals, and many microbial associations are transient rather than vertically transmitted. The current consensus treats the holobiont as a useful ecological concept — organisms and their microbiomes do function as integrated physiological units — while remaining cautious about treating it as a unit of selection in the strict evolutionary sense.

Related

• Symbiosis — the associations that constitute holobiont organization
• Homeostasis — maintained across species boundaries within the holobiont
• Niche Construction — holobionts as niche constructors at micro and macro scales
• Fungal Symbiosis — lichens and mycorrhizae as holobionts
• Mycelial Networks — network-scale connections between holobionts