An ancient symbiosis founded entirely on exploitation, not mutual benefit

January 4, 2016, University of Exeter
An ancient symbiosis founded entirely on exploitation, not mutual benefit
Scientists have been debating for decades whether symbioses, like the Paramecium-Chlorella association, are based on mutual benefit or exploitation.

Biologists at the universities of Exeter and York have published new research which shows that an ancient symbiosis is founded entirely on exploitation, not mutual benefit.

The researchers concluded that a single-celled protozoa called Paramecium bursaria benefits from exploiting a which lives inside it, providing its host with sugar and oxygen from photosynthesis.

Scientists have been debating for decades whether symbioses, like the Paramecium-Chlorella association, are based on mutual benefit or exploitation.

The common belief among academics was that both the protozoa and benefit.

Dr Chris Lowe, lecturer in Evolutionary Ecology at the University of Exeter and lead researcher on the paper, said: "This research suggests that what we have always thought of as mutualism – where species gain from interacting with each other – might actually be based on exploitation where one species gains by capturing and then taking resources from another."

The new research builds on work carried out 20 years ago at the University of York by Professor Richard Law.

Professor Mike Brockhurst, from the Department of Biology, said: "Richard Law came up with exploitation theory in the 1990s and his mathematics has shown to be correct.

"This new research has turned the assumption that symbiosis is mutually beneficial on its head."

Professor Brockhurst said the team, which also included researchers from the University of Sheffield, tested the symbiotic relationship of the protozoa and algae across gradients of different .

"We found that for the host the benefits of being in symbiosis increased with light. Although symbiosis is very costly in the dark for the hosts, because the algae are useless, when you increase the light intensity then it becomes very beneficial to have algae because they give you lots of sugar.

"Across all of the environments that we tested we never found any conditions where both species benefited. For the algae it is always costly to be in symbiosis."

Professor Brockhurst said the research, which was funded by the Natural Environment Research Council (NERC) and published in Current Biology, suggests there is likely to be an exploitative component in other symbiotic relationships.

"The big one is corals, where climate change related bleaching results from loss of photosynthetic microbial symbionts," he added.

"I suspect in a lot of cases where we assume mutualism we might find that isn't the case, which has important implications for understanding and conserving symbioses in nature.

"Because symbioses are so common, understanding how symbiotic species interact and how they evolve will tell us a lot about ecosystems and how they will respond to climate change."

Explore further: Response to environmental change depends on individual variation in partnership between corals and algae

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3 / 5 (1) Jan 04, 2016
And might this arrangement be expanded to include higher life forms?
5 / 5 (3) Jan 04, 2016
@KS - yes. Giant clams harbor photosynthetic symbionts, for example.
5 / 5 (2) Jan 05, 2016
Yes, the article implies the scientists think it is a general mechanism ("a lot of cases"). It will be controversial and how the chip comes down is iffy to say.

Though I note that population genetics of 'selfish' genes can easily predict forms of cooperation (such as symbiosis) up to kinship altruism, but the basis for mutualism is a putative ecological mechanism. [ https://en.wikipe...biology) ] This work would tend to draw an area into classical evolutionary biology.
5 / 5 (1) Jan 05, 2016
I think the result and its implication is promising. Not only simplifying the biology and putting it on solid ground, it is consistent with the latest mitochondrial tree where the pre-mitochondrion was found to be a parasite. A Lokiarcheon engulfed them but eventually couldn't digest them, likely due to some evolved defense. Instead it took likely millions of years for the now eukaryote to defang the obligate parasite and turn the now endosymbiont from the master into a slave.

Repeating the procedure with the far less dangerous cyanobacteria to become an algae, and yet again (from the Paramecium's perspective) to become a Paramecium-Chlorella association, would be simple in comparison.
3 / 5 (1) Jan 05, 2016
The claim this "ancient symbiosis is founded entirely on exploitation, not mutual benefit" is grossly exaggerated and misleading.

The article does concede, "Although none of the environmental conditions used here resulted in mutual benefits of nutrient exchange, it is possible that other environmental factors, like parasitism or predation". But to relegate the predation on Chlorella by larger protists or parasitism by smaller viruses to mere 'possible' benefits of their endosymbiosis with Paramecium bursaria is a ridiculous understatement, and should be better reflected in the conclusions from this small study.

The authors also make a huge assumption by claiming evolutionary stability can be understood through the measure of each partner's individual fitness – when evolutionary stability of a symbiosis relies just as much (if not more) about each their individual and collective resilience against different stresses, such as disease or predation.
not rated yet Jan 06, 2016
The article seems to sum up the (open access!) paper well. Its higligt claims "Symbiosis is always costly for algae".

The paper did check the relative fitness loss with free living Chlorella, with or without the provision of nitrogen that was believed to be the major benefit in endosymbiosis. The environments were neither sterile nor as complex re parasitism and predation as "more complex natural environments" so "this will be a focus of future experiments". But they did identify a regime were "host-symbiont conflicts" was a problem, and they propose that it is a likely problem when transitioning "from facultative to obligate symbiosis".

not rated yet Jan 06, 2016

I don't get the last part of your criticism, but I am no biologist. Here is my problem: having selfish genes means organisms, having some differing alleles in the sense of different organism lineages, are orthogonal (in the mathematical sense* applied to population genetics) under fitness.

My layman, naive understanding of the ecological mechanism is that it constrains organisms so the fitness effects are mutual, analogous to how germ and soma cell lineages cooperate due to sharing alleles. But if it isn't there, a "collective resilience" is not there.

*I haven't seen a formal result. But it seems to me I could put alleles as vectors in a matrix space of strand sequences (say), and the result should follow for theoretical 'organisms' (vectors) after orthogonalization.

The practical idea is that different organisms behave differently in some environments, they have differing traits and that reflects on fitness.
not rated yet Jan 06, 2016
Torbjorn, for a non-biologist, you have an outstanding understanding of biology and fitness!

My main problem with the paper is simple.
One the one hand, I think the researchers have chosen a great symbiotic relationship to explore and really like the experimental approach and results.
However, I also believe these early experiments simply do not warrant the sensational conclusion: "symbiosis founded ENTIRELY on exploitation".
Scientists and science communicators have a duty to report the uncertainties in their results in an honest and straightforward manner...and as such, the use of the word 'entirely' here is completely innapproproate and misleading!

That said, I look forward to seeing future results from these researchers, as they attempt to model more realistic natural environments (hopefully involving some metagenome and transcriptome analysis of the symbiotic partners)...after which I am confident they will have to eat the word 'entirely'.

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