Endosymbiosis is fundamental to multicellular life since all multicellular organisms are collections of eukaryote cells, which are themselves alliances of prokaryote cells i an endosymbiotic relationship.
It illustrates as well and any other evolved cooperative alliances how natural selection, which make genes look like they are relentlessly selfish and the deadly rivals of other alleles of the same gene, often results not in rivalry and competition but alliances and cooperation.
However, for one cell to enter another cell, take up residence in it and be transmitted vertically from one generation to the next, as must have happened with the earliest eukaryote cells, a number of barriers must be overcome, not the least of which is that a cell with a potentially parasitic organism inside it is either going to try to reject it or be less efficient, therefore less competitive, then uninfected cells and would tend to be eliminated in the struggle to succeed.
Tell me about endosymbiosis and the barriers that needed to be overcome for it to succeed. Endosymbiosis is the process in which one organism lives inside the cells or body of another organism in a mutually beneficial relationship. The most famous example is the origin of mitochondria and chloroplasts in eukaryotic cells. According to the endosymbiotic theory, these organelles originated from free-living prokaryotes (bacteria) that were engulfed by ancestral eukaryotic cells. Over time, these symbionts became integrated into the host cell and provided essential functions, such as energy production (mitochondria) or photosynthesis (chloroplasts).Now however, a group of researchers led by Julia Vorholt, Professor of Microbiology at Eidgenössische Technische Hochschule (ETH) Zurich, have shown how some of these barriers may have been overcome in the early history of life on Earth.
For endosymbiosis to succeed, several significant barriers had to be overcome:
- Recognition and Compatibility
- Avoidance of Immune Rejection: The host cell had to recognize the engulfed prokaryote as beneficial rather than as a pathogen to be destroyed. Early interactions between host and symbiont would have required mechanisms to avoid immune responses.
- Membrane Fusion and Maintenance: The engulfed organism had to be enclosed within the host's membrane system without being digested. Membrane fusion and maintenance were critical to ensure the symbiont’s survival inside the host.
- Stable Coexistence
- Nutrient Sharing: The symbiont needed to supply the host with beneficial products (e.g., ATP from mitochondria or organic carbon from chloroplasts), while the host provided raw materials or protection in return. Establishing a stable exchange of nutrients required metabolic integration.
- Reduction of Redundancies: Over time, some genes in the symbiont were transferred to the host genome, reducing the redundancy of having two sets of genes for similar functions. This allowed for tighter control and coordination between the host and the symbiont.
- Genetic Integration
- Gene Transfer: One key barrier was the transfer of essential genes from the symbiont’s genome to the host’s nucleus. This process ensured that the host could regulate the symbiont's functions, while the symbiont’s genome became streamlined. Most mitochondrial and chloroplast genes are now part of the host genome, though the organelles retain some of their own DNA.
- Coordination of Gene Expression: The host cell had to evolve mechanisms to coordinate gene expression between the nucleus (containing host and transferred symbiont genes) and the organelle. This involves the synthesis of proteins in the host cell that are then transported into the organelle for proper functioning.
- Replication and Transmission
- Symbiont Replication Synchronization: For endosymbiosis to be stable, the symbiont’s replication cycle needed to be synchronized with that of the host cell. This ensured that both the host and the symbiont were inherited together during cell division.
- Vertical Transmission: Successful endosymbiosis required the symbiont to be passed from one generation to the next, typically through maternal inheritance (e.g., mitochondria are inherited from the mother). This guaranteed that the endosymbiotic relationship was maintained across generations.
- Evolutionary Stability
- Mutual Dependency: Over evolutionary time, both the host and the symbiont became highly dependent on each other for survival. This mutual dependency helped ensure that the relationship persisted, as neither could function optimally without the other.
- Loss of Autonomy: The symbiont gradually lost the ability to survive independently. As more genes were transferred to the host genome, the symbiont became an integrated organelle rather than an independent organism.
Endosymbiosis is a powerful example of how cooperation and integration between different life forms can lead to major evolutionary innovations, allowing for greater complexity and specialization in life on Earth.
Their findings have just been published, open access, in the journal Nature and explained in an ETH Zurich news release:
How a bacterium becomes a permanent resident in a fungus
An organism as a tenant in another - in biology, this often works quite well. ETH researchers have now shed light on how such a partnership of a cell in a cell can establish.
In briefEndosymbiosis is a fascinating biological phenomenon in which an organism lives inside another. Such an unusual relationship is often beneficial for both parties. Even in our bodies, we find remnants of such cohabitation: mitochondria, the powerhouses of our cells, evolved from an ancient endosymbiosis. Long ago, bacteria entered other cells and stayed. This coexistence laid the foundation for mitochondria and thus the cells of plants, animals, and fungi.
- ETH researchers investigated the beginning of endosymbiosis, the stable coexistence of a bacterium in a fungus. To do this, they injected bacteria into cells of a fungus.
- They observed that the implanted bacteria were able to both multiply within the host cells and be passed on to the next generation.
- The cohabiting partners adapted to each other and eventually both benefited.
What is still poorly understood, however, is how an endosymbiosis as a lifestyle actually arises. A bacterium that more or less accidentally ends up in a completely different host cell generally has a hard time. It needs to survive, multiply, and be passed on to the next generation. Otherwise, it dies out. And to not harm the host, it must not claim too many nutrients for itself and grow too quickly. In other words, if the host and its resident cannot get along, the relationship ends.
To study the beginnings of such a special relationship between two organisms, a team of researchers led by Julia Vorholt, Professor of Microbiology at ETH Zurich, initiated such partnerships in the laboratory. The scientists observed what exactly happens at the beginning of a possible endosymbiosis. They have just published their study in the scientific journal Nature.
The fact that the bacteria are actually transmitted to the next generation of fungi via the spores was a breakthrough in our research.
Gabriel H. Giger, first author
Institute of Microbiology
Department of Biology
ETH Zurich, Zurich, Switzerland.
Enforcing cohabitation
For this work, Gabriel Giger, a doctoral student in Vorholt's laboratory, first developed a method to inject bacteria into cells of the fungus Rhizopus microsporus without destroying them. He used E. coli bacteria on the one hand and bacteria of the genus Mycetohabitans on the other. The latter are natural endosymbionts of another Rhizopus fungus. For the experiment, however, the researchers used a strain that does not form an endosymbiosis in nature. Giger then observed what happened to the enforced cohabitation under the microscope.
After the injection of the E. coli bacteria, both the fungus and the bacteria continued to grow, the latter eventually so rapidly that the fungus mounted an immune response against the bacteria. The fungus protected itself from the bacteria by encapsulating them. This prevented the bacteria from being passed on to the next generation of fungi.
Bacteria enter the spores
This was not the case with the injected Mycetohabitans bacteria: While the fungus was forming spores, some of the bacteria managed to get into them and thus were passed on to the next generation.
When the doctoral student allowed the spores with the resident bacteria to germinate, he found that they germinated less frequently and that the young fungi grew more slowly than without them. “The endosymbiosis initially lowered the general fitness of the affected fungi,” he explains. Giger continued the experiment over several generations of fungi, deliberately selecting those fungi whose spores contained bacteria. This enabled the fungus to recover and produce more inhabited but viable spores. As the researchers were able to show with genetic analyses, the fungus changed during this experiment and adapted to its resident.
The researchers also found that the resident, together with its host, produced biologically active molecules that could help the host obtain nutrients and defend itself against predators such as nematodes or amoebae. “The initial disadvantage can thus become an advantage,” emphasizes Vorholt.Fragile systemsVideo: ETH Zurichfrom Giger GH, et al, Nature 2024.
In their study, the researchers show how fragile early endosymbiotic systems are.
The prerequisite for this is that the prospective resident brings with it properties that favor endosymbiosis. For the host, it is an opportunity to acquire new characteristics in one swoop by incorporating another organism, even if it requires adaptations.The fact that the host's fitness initially declines could mean the early demise of such a system under natural conditions. For new endosymbioses to arise and stabilize, there needs to be an advantage to living together. In evolution, endosymbioses have shown how successful they ultimately can become.
Professor Julia A. Vorholt, Corresponding author
Institute of Microbiology
Department of Biology
ETH Zurich, Zurich, Switzerland.
ReferenceGiger GH, Ernst C, Richter I, et al.
Inducing novel endosymbioses by implanting bacteria in fungi. Nature, 02 October 2024, doi:10.1038/s41586-024-08010-x
AbstractEndosymbiosis is a typical Heath-Robinson solution to a problem produced by the unintelligent, unplanned, utilitarian process of evolution. It is the opposite of what an intelligent design process with an objective would produce because it would not be beyond the wit of an intelligent designer to give a cell all the required capabilities from the start. The fact that the result is a complex cell, not a comparatively simple one, is evidence not of intelligent design but a lack of intelligence in the process, since good design is minimally complex.
Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification1,2. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect3,4,5. Here we implant bacteria into the filamentous fungus Rhizopus microsporus to follow the fate of artificially induced endosymbioses. Whereas Escherichia coli implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis, Mycetohabitans rhizoxinica was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
Main
Intracellular endosymbioses are extraordinarily intimate interactions between organisms. They join two complex metabolic networks in a compartmentalized manner and are subjected to natural selection as a unit. This metabolic integration predisposes endosymbioses to enable major transitions in evolution1,2. Accommodating an endosymbiont can benefit the host by acquiring chemical defence systems and unlocking essential nutrients or new energy sources2,6,7,8. However, many obstacles limit de novo endosymbiogenesis3,4,5. Besides the first hurdle of host cell entry, a prospective endosymbiont must overcome challenges associated with immune responses, metabolism and growth synchronization3,9,10. Even if the combined metabolisms theoretically sustain growth in silico11, unstable outcomes are the prevailing norm, failing to stabilize vertical transmission11,12.
Studying established natural partnerships has provided insights into the intricate interactions of extant endosymbioses. These include mitochondria and chloroplasts as relicts of ancient bacterial endosymbionts, as well as insect endosymbionts that have long been vertically transmitted and have undergone genome reduction13. However, shifting balances of control between the partners, phases of stabilization and destabilization and equivocal lines between mutualism and antagonism blur evolutionary trajectories13,14,15,16. Consequently, the earliest steps in endosymbiogenesis remain difficult to uncover15. Synthetic approaches can provide well-defined starting points to follow stable and unstable outcomes. Interventional studies have focused mainly on insects, in which transinfection has revealed important aspects of endosymbiogenesis, such as control of bacterial replication17,18 and metabolic cooperation19,20. However, attempts in other phyla, such as installing engineered E. coli or cyanobacteria in yeast21,22, have not resulted in stable endosymbiosis under strict selection.
Here we set out to generate a novel endosymbiotic partnership in a non-host filamentous fungus. The model system consisted of the early divergent fungus Rhizopus microsporus and the cytosolic bacterial endosymbiont Mycetohabitans rhizoxinica23,24. Certain host strains of R. microsporus contain Mycetohabitans endosymbionts25. In these, vertical inheritance is strict, as the fungus cannot sporulate without the endosymbiont, which reliably colonizes the spores26,27. This probably drives co-diversification25. The association is presumed mutually beneficial28, with bacterially produced rhizoxin congeners29,30 providing the fungus fitness advantages by protecting against amoeba and nematodes31, and aiding in nutrient acquisition by causing rice seedling blight23. Both partners can be cultured axenically, and host strains cured from the endosymbiont are readily reinfected by M. rhizoxinica26,32. By contrast, non-host strains resist natural colonization and do not require endosymbionts for sporangiospore formation33,34. For this study, R. microsporus strain EH (endosymbiont-harbouring) and strain NH (non-harbouring) were used.
To study initial endosymbiogenesis events, we used single-cell approaches to observe cellular responses before environmental selection could act. Fluidic force microscopy (FluidFM)35 was recently adapted to inject bacteria into mammalian cells, bypassing cellular entry steps and enabling evaluation of engineered pairs to test intracellular growth36,37. Applying this technique to fungi is challenging owing to the complexity of fungal mycelia, the rigid cell wall and high turgor pressure38,39. In this work, we report a procedure to implant bacteria into R. microsporus that enabled real-time tracking using confocal microscopy and characterizing early adaptations in the endosymbiosis under stabilizing selection pressure.
Giger, G.H., Ernst, C., Richter, I. et al.
Inducing novel endosymbioses by implanting bacteria in fungi. Nature (2024). https://doi.org/10.1038/s41586-024-08010-x
Copyright: © 2024 The authors.
Published by Springer Nature Ltd. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
The unplanned, essentially haphazard 'trial and error' process of evolution, driven by environmental selectors, will always settle for whatever was better than its predecessor, regardless of how inefficient and wasteful it might be.
Combined with the fact that cooperation is often more beneficial to all participants in a cooperative arrangement, evolution frequently results in increasingly complex cooperative alliances whether as single eukaryote cells, multicellular organisms or whole ecosystems, exactly as the Theory of Evolution by Natural Selection predicts.
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