Partner Selection and Partner Exchange Between Power Struggle and Dependency

Stability Through Transformation

An article from carl 03|2025
by Karin Hollricher

Evolutionary adaptation means nothing stays as it is. The same applies to endosymbioses. The parties choose each other according to their current needs. If the requirements change, the symbiont must either adapt or the host will look for a different partner.

Endosymbioses are among the most stable mutualistic partnerships. In many cases, after centuries of adaptation, the partners can no longer survive without each other. For example, plants are dependent on their chloroplasts, whose ancestors were once cyanobacteria that existed independently. A team from the University of Illinois in Urbana-Champaign has attempted to replicate the start of this kind of partnership in a lab by injecting cyanobacteria into yeast cells. The question was: Is the interdependency produced in the lab stable? This would be the prerequisite for the start of an endosymbiotic relationship. In fact, the bacteria stayed in the cells for up to twenty yeast generations [1]. It is possible that the yeast benefits from the photosynthetic bacteria, because it was observed that the yeast reproduced faster in the light than in the dark – which is not usual in standard yeast. This is now the subject of current research.

Leaf cells of the moss Bryum capillare with chloroplasts

But how does an endosymbiotic relationship develop under natural conditions? One hypothesis is that it develops from the parasitic interaction between a microorganism and its host. The condition for this would be that the conflict for resources between the two parties is controllable, with the partners neither killing each other nor impairing their fitness to such an extent that one or both are destroyed in the course of evolution. Empirically, such events – i.e. the transformation from parasitic to mutualistic – can actually be proven in yeast-like fungi that live in various cicada species. Genome comparisons with relatives show that these fungi stem from parasitic forms [2, 3].

Is an endosymbiosis the result of a tamed conflict then?

This theory is supported by the renowned symbiosis researchers Patrick Keeling (University of British Columbia, Vancouver) and John McCutcheon (Arizona State University). They interpret endosymbioses as rather one-sided associations “…that can be viewed as context-dependent power struggles, in the same way as every other ecological interaction.” [4] This type of power struggle can be observed in the co-existence of the mould fungus Rhizopus microsporus with the bacterium Mycetohabitans rhizoxinica. Neither the fungus nor the bacteria depend on each other for survival; the fungus can be found in many habitats even without these microbes. Only one strain appears to be dependent on the bacteria, but does not really tolerate them voluntarily, as discovered by researchers from the Hans Knöll Institute in Jena [5]. This strain of the fungus lives parasitically on rice plants; the bacterium helps it to do this by producing a potent cytotoxin called rhizoxin. The fungus is immune to this, but the cells of rice plants are not. In addition, the fungus requires its co-resident for asexual reproduction: without M. rhizoxinica, it cannot form spores. The cause of this is not yet known.

Fluorescence imaging of Mycetohabitans-rhizoxinica bacteria (green) in fungal hyphae (blue) [5]

Despite these obvious advantages, the fungus only accepts its co-residents reluctantly. If, for example, the bacteria cannot produce a certain protein, the host actively defends itself and kills them. The protein in question is a TAL effector – a class of molecules that control gene expression. How the bacterium uses this to paralyse the host’s natural defences is now being investigated.

Researchers at ETH Zürich are attempting to find out why not all strains of R. microsporus host bacteria. They infect individual cells of hosts and non-hosts with bacteria and leave them to run through an artificial evolution process [6]. Only the fungal spores that contained the bacteria were found to reproduce. In the non-hosts, the new endosymbionts were at first found to significantly impair the asexual reproduction of the fungi, measured as the germination rate of the spores. With increasing rounds of selection and reproduction, however, this effect lessened. At the same time, special mutations occurred in the fungi. The researchers are interpreting these results as evolutionary adaptation of the non-hosts.

Do endosymbioses last forever, once they are established? No, because even cooperative relationships are subject to the laws of evolution and break down if one of the partners finds a more suitable companion for the respective circumstances. No matter how long a symbiosis has already existed for, it will change under the influence of changing environmental conditions and the associated pressure for selection. This can be seen, for example, in the loss of mitochondria.

Schematic drawing of an animal cell. Mitochondria are shown in blue.

According to text books, every eukaryotic cell should carry mitochondria, because these organelles provide energy in the form of the molecule ATP. Mitochondria are considered to be endosymbionts because, like chloroplasts, they evolved from bacteria that were once absorbed by single-cell organisms. Surprisingly, however, researchers have now found a eukaryote in the flagellate Monocercomonoides that can get by without mitochondria [7].

This was just the first example of such an “amitochondrial” life form: the representatives of the very species-diverse strain of metamonada can also exist without fully functioning mitochondria. In all previously investigated species, only “mitochondria-related organelles” (MROs) in various stages of degradation were found. Metamonada are single-cell organisms that live in anaerobic environments, such as the digestive tract of animals or in deep water. Some MROs can even synthesise ATP, although without using oxygen. Other MROs have passed ATP production on to the host cell. While mitochondria reduce themselves down to MROs, they, like their hosts, lose the genes they require for aerobic metabolism. Instead, the hosts have incorporated genes from other microorganisms that enable the production of ATP through other biochemical methods. One species, Skoliomonas litria, has completely lost its mitochondria, as reported by researchers from Dalhousie University in Halifax [8].

Illustration of the endosymbiont Candidatus Azoamicus ciliaticola and its host, a ciliate (superimposed images from fluorescence and environmental scanning electron microscope). C. A. ciliaticola (yellow) and bacterial spoils in food vacuoles, cell nucleus of the ciliate (blue) [9].

To date, it has not been possible to find out how amitochondrial metamonada and flagellates produce ATP. But we do know how a ciliate survives without mitochondria. In the depths of Zug Lake in Switzerland, a cooperation team from the Max Planck Institute for Marine Microbiology in Bremen, the Max Planck Genome Centre in Cologne and the Swiss Eawag water research institute, made a discovery. As part of a metagenome analysis, scientists found genes that are required for nitrate oxidation but which are also unusual for organisms living in deep waters and oceans. It turned out that these genes stemmed from a bacteria called Candidatus Azoamicus ciliaticola, which lives as an endosymbiont in a ciliate [10]. Normally, bacteria are a ciliate’s favourite food – but in this case, it entered into a mutualistic symbiosis with a microbe. This is the first report of a new endosymbiont taking on the function of mitochondria, namely the production of ATP. The special partnership enables the flagellate to conquer a new – oxygen-free – habitat. The researchers see this as a strong sign that nature still holds more fascinating and yet-to-bediscovered mutualistic lifeforms.

Evolution of a cooperation: from endosymbiont to organelle

The marine, single-cell algae Braarudosphaera bigelowii in its form as a soft-bodied flagellate (syn. Chrysochromulina parkeae), microscopic photography (left, without endosymbiont) and schematic drawing (right, with endosymbiont in the posterior end). Colouring of the organelles: nitroplast UCYN-A cyan, cell nucleus pink and chloroplasts green.

Mitochondria and chloroplasts emerged from endosymbiotic bacteria. They are classified as organelles, because they surrendered genes to the cell nucleus of the host, their metabolism is strongly linked with that of their host and their reproduction is subject to the control of the host cell. The endosymbiotic bacterium Atelocyanobacterium thalassa (UCYN-A), which lives in B. bigelowii and its close relatives, also behaves like an organelle. This was discovered by researchers at the University of California in Santa Cruz (UCSC) and colleagues, after they successfully cultivated this symbiotic community in the lab. Genome and proteome analyses as well as X-ray microscopy (SXM) showed that UCYN-A imports essential proteins produced by the host and divides itself in sync with the host’s mitochondria and chloroplasts [11]. Due to its nitrogen-fixing properties, UCYN-A is now referred to as a nitroplast.

Glossary

Nucleotide ATP (adenosine triphosphate) is the universal source of energy in cells.

The metagenome is the entirety of the genomes of all microorganisms in a habitat.

[1] J. Cournoyer et al., 2022, Nature Commun. 13, 2254
[2] Y. Matsuura et al., 2018, PNAS 115, e5970-e5979
[3] R. Siehl, et al., 2024, iScience 27, 110674
[4] P. Keeling und J. McCutcheon, 2017, J. Theor. Biol. 434, 75-79
[5] I. Richter et al., 2023, Current Biol. 33, 2646-2656
[6] G. Giger et al., 2024, Nature 635, 415-422
[7] L. Novak et al., 2023, PLoS Genet. 19, e1011050
[8] S. Williams et al., 2024, Nature Commun. doi.org/10.1038/s41467-024-50991-3
[9] www.mpi-bremen.de/Neue-Form-der-Symbiose-entdeckt.html
[10] J. Graf et al., 2021, Nature 591, 445-450, doi.org/10.1038/s41586-021-03297-6
[11] T. Coale et al., 2024, Science 384, 217-222, doi.org/10.1126/science.adk1075

Image credits: Wikimedia Commons, Des_Callaghan / Ingrid Richter, Leibniz-HKI / Adobe Stock, GraphicsRF / S. Ahmerkamp, © Max-Planck-Institut für Marine Mikrobiologie, Bremen / Wikimedia Commons, Mats & Maria Kuylenstierna, Bengt Karlson (University of Gothenburg, Marine botany, via SMHI) / die Komplizen

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