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Does the Holobiont Add Crucial Context or Irrelevant Complexity?

Oct. 1, 2021

It may be comforting to think of organisms as more than the sum of their parts. Though there is much still to learn about microbiomes, it is clear that human health and wellbeing relies on more than those cells described by human DNA. It has always been this way: from an evolutionary perspective, plants and animals are guests in a bustling microbial world. Enter the holobiont.
 
The concept of the holobiont extends a central organism, like a human being, to include the consortium of microorganisms in, on and around it. Holobiont theory recognizes the unseen wrinkle of microbial life, then folds it back into an observable eukaryote. Considering this, the concept of holobionts allows people to appreciate eukaryotic organisms in a fuller context that challenges evolutionary theory by allowing the branches of the tree of life to intersect.
 
Holobionts, and their collective hologenomes, are a topic of debate among scientists, but this concept has certainly taken hold in the modern evolutionary lexicon. With this understanding, it is no simple task to determine where an organism ends, and the outside world begins. What is driving the holobiont idea? What are the benefits and limitations of this holistic perspective?

The Mitochondrion in the Room

The concept of the holobiont was initially championed by Dr. Lynn Margulis in the 1990s. She popularized the concept in her book . This career-defining work was a natural extension of her early interests in the origin of eukaryotic cells. This existential origin puzzle examines how eukaryotic cells came to be and sits squarely in the field of symbiogenesis.
 
Symbiosis is when organisms live together, and symbiogenesis is a major evolutionary event where symbioses become so intertwined that they generate a new organism entirely. Organisms that have undergone symbiogeneses, which includes all eukaryotic life, are members of a holobiont that have both committed over a long period of time to becoming one.

History of symbiosis, endosymbiosis and holobiont concepts from 1800s to today.
History of symbiosis, endosymbiosis and holobiont concepts from the 1800s to today.
Source:
 

This field of symbiont-gazing is an important precedent for understanding the modern concept of a holobiont, because most holobionts are scaffolded around a charismatic eukaryote. Looking back far enough in the history of eukaryotes, their archaean ancestors once courted free-living mitochondrial ancestors. It is worth noting that the origin of the term “holobiont” is attributed to , who himself was grappling with the nature of symbiosis. These scientists led the trend of symbiologists questioning single organisms as the central unit of biology as they fell deeper into the symbiotic rabbit hole.

Corals as Holobionts

A variety of corals form an outcrop on Flynn Reef, part of the Great Barrier Reef near Cairns, Queensland, Australia.
A variety of corals form an outcrop on Flynn Reef, part of the Great Barrier Reef near Cairns, Queensland, Australia.
Source:
Perhaps the best-known case for holobionts is coral. Corals are partnerships between an animal (what one would physically see as a coral) and algae (called zooxanthellea). Aside from adding a serious pop of color, these photosynthetic algae turn light into sugar for the animal partner to eat. The algal role is critical to the coral enterprise. Before this discovery, corals were thought to be wholly one organism.
 
In this way, considering corals as holobionts that encompass both the animal and its microscopic partner is not a new paradigm; rather, it’s a refinement of our previous understanding of what makes an individual coral polyp.

Lichens as Holobionts

This Cladonia lichen is a holobiont that includes a mycobiont (a fungus), a photobiont (alga) and all other associated microbes.
This Cladonia lichen is a holobiont that includes a mycobiont (a fungus), a photobiont (alga) and all other associated microbes.
Source: Brian Lovett
Lichenology is another field that has adopted the concept of holobionts. Here too, the role of photosynthetic microbes (supported by symbiotic fungi) was uncovered. In this system, the mycobiont (typically an ascomycotan fungus) helps collect minerals and nutrients and provides a safe place for the photobiont (algae or cyanobacteria) to photosynthesize sugar. The complex mosaic of this system cannot be understated, and researchers recently discovered that .
 
Just a square inch of bark can contain a handful of lichen, and the evolutionary history of each of these holobionts is (at least) a 2-part volume. Specifically, how each partner in this symbiosis came to be and how they formed their symbiosis is an important context for describing and studying lichen. , and these complex interactions cannot be unraveled looking at the mycobiont alone. Viewing lichens as holobionts adds value to this scientific system by appropriately framing their evolution and providing full context for observations about individual lichens.

Mosquitoes as Holobionts

Mosquitoes too can be considered holobionts. Intracellular bacteria in the genus Wolbachia can variously alter the reproduction of insects. Many insects naturally harbor Wolbachia in their cells. Wherever Wolbachia species lie along the symbiotic spectrum with their host (from parasite to mutualist), they can still be considered part of the mosquito holobiont. These bacteria cause a phenomenon called cytoplasmic incompatibility in mosquitoes, which affects whether sperm and eggs can successfully develop into a mosquito. Males with this bacterium can . Females carrying this bacterium can mate with whomever and pass the bacterium to their offspring.
 
This bacterial manipulation of mosquito reproduction ensures the bacterium is passed onto the next generation by limiting mosquito mating success. Wolbachia can also alter a mosquito’s ability to harbor and transmit infectious pathogens like dengue virus. Without knowing the Wolbachia status of a mosquito, it is difficult to predict with whom it can mate or the diseases it can carry. These natural abilities of Wolbachia have led to that are less likely to transmit pathogens.
 
The mosquito-based holobiont encompasses more than Wolbachia. In order to develop, a mosquito must have gut bacteria. Bacteria naturally consume oxygen in the gut: is required for successful mosquito molting. Intriguingly, these researchers found that bacteria that aren’t normal members of the mosquito gut community can provide this stimulus. For these experiments at least, this strange microbe became a crucial cog of the mosquito holobiont.

When Is a Humble Biont Enough?

Though intricate symbioses are all around us, . Proponents of this idea argue that our understanding of evolution is incomplete until it can accommodate events that forge new holobionts. Holobionts are so named because they consider microbial life and so are more “whole.” However, this additional information can present practical challenges that are familiar to scientists who wade through microbiomes—who is doing what and how do they contribute to the whole? For now, anyway, the complexity and ephemerality of the microbial world has left most holobionts undescribed.
 
Holobionts are assembled around a larger, multicellular eukaryote. These symbiotes could be any other form of microbial life and may interact with the hosting eukaryote in unique ways. , by contrast, is fermented by a symbiotic consortium of bacteria and yeasts (known as a SCOBY). This consortium lacks a central eukaryote, so researchers understand and study it as a microbial community, rather than a true holobiont.
 
Even if one considers holobionts to be , there will be questions where it’s best to focus in further. Reducing variables to the essential for an experiment can often provide the best insight into subtle phenomena. This often requires isolating organisms unnaturally. However, myopic viewpoints can be deceiving. The development of holobiont theory reflects a larger desire to appreciate the messiness of biology more fully. 

Author: Brian Lovett, Ph.D.

Brian Lovett, Ph.D.
Brian Lovett is a postdoctoral researcher working on fungal biology and biotechnology at West Virginia University.