TLDR; Here, we'll be looking into whether methanogens could give rise to complex life on other planets. We also look into how this unfamiliar form of life may develop, leading to some interesting results.
Recently, I was browsing through the official speculative evolution discord server and came across an interesting question. In it, Silly_Milly asks whether or not methanogensis (the coupling of hydrogen / acetate / methyl oxidation with the reduction of CO2) could provide enough energy to support "eukaryote like complexity". In other words, would methanogenesis allow microbes to achieve larger genome sizes?
However, in order to answer their question, we first have to ask ourselves why eukaryotes are able to support large genome sizes in the first place. As many of you might know, the answer is mitochondria.
Roughly 2.1 billion years ago, the common ancestor of mitochondria had forged an mutualistic arrangement with an archaeal host. This provided them with shelter from the elements and from competition.
Since they no longer had to invest energy towards supporting an active, free-living lifestyle, mitochondria have undergone a dramatic reduction in genome size and have greatly decreased their rate of ATP consumption. However, their overall rate of ATP production had remained the same, providing them with far more energy then they knew what to do with.
Instead of stockpiling this excess ATP for themselves, populations of mitochondria work together, exporting it and donating it to their hosts. This increase in stored energy would have allowed early eukaryotes to develop more costly adaptations that would serve to increase the reproductive fitness of both the host and the endosymbionts. In addition, mitochondrial populations can be scaled up in order to keep up with the energetic demands placed upon them by their host, enabling eukaryotes to support genomes of progressively greater size and relative complexity.
So to simplify, the reason eukaryotes are able to harbor large genomes has more to do with how mitochondria allow them to efficiently scale up energy production, rather than something that is unique to aerobic respiration.
Therefore, if we were to imagine a hypothetical, eukaryote-like cell with methanogens in place of our oxygen reducing / lactic acid fermenting mitochondria, they would still be able to function in a similar manner to their real-life counterparts. However, since methanogenesis produces ATP yields that are far lower than that aerobic respiration (0.5-2 moles of ATP per mole of substrate Vs. the 30-32 moles of ATP generated from the aerobic consumption of one mole of pyruvate), a greater number of methanogens would be required to produce the same amount of ATP. As a result, "methano-eukaryotes" would have to obtain far more resources and chemical energy from their environment than true-eukaryotes would in order to achieve similar energy budgets.
With that said, plenty of eukaryotic cells on the modern day Earth support populations of mitochondria numbering in the thousands, so its well within the realm of possibility that our methano-eukaryote could harbor large populations of endosymbionts as well. However, it's also important to note that the caloric and nutritive demands mitochondria place upon their hosts had once played an important role in stalling their evolutionary development of eukaryotes throughout much of the Proterozoic, back when essential biogenic elements and oxygen were more difficult to come by. Because of this, methano-eukaryotes on similarly nutrient-starved exoplanets would have an even greater challenge diversifying and developing costly adaptations.
Additionally, the presence of oxygenic photosynthesis on alien planets will largely restrict methanogens to anoxic sediments and other environments that greatly limit the availability of oxygen, such as geothermal springs. However, in a recent study published in 2011, researchers found that methanogens in the McMurdo Dry River Valley can survive in oxygenated soils by upregulating the detoxification of oxygen and ROS (reactive oxygen species). This uses up a significant portion of their meager energy budget, but seems to enable them to slowly metabolize, grow, and reproduce within aerobic environments.
*NOTE : Due to our hypothetical microbe's ability to scale up respiration, they would have more than enough energy to invest in upregulating these processes. Because of this, they might still be able to support relatively fast rates of cell division under oxygenated conditions. Additionally, there's also the chance that the host might start out as a facultative aerobe, much like how mitochondria did. This would allow them to potentially shield their endosymbionts from oxygen, either through the consumption of oxygen during respiration or the use of their own detoxification pathways.
Another problem we have to address involves the substrates required for methanogenesis. In aerobic environments, hydrogen gas is in limited supply and is often restricted to the presence of trace gases. While organisms use radiolytic hydrogen in the atmosphere for growth, the energy this provides is incredibly meager and only serves to supplement the cell's ATP requirements. As a result, I wouldn't expect a eukaryote-analogue to thrive primarily off of hydrogen in an aerobic habitat. Instead, acetate and methylated compounds might serve as better donors, since they can be easily sourced from detritus.
Alternatively, the host cell could have originally started out with the ability to produce its own acetate from more abundant carbon sources in the environment, thereby providing their endosymbionts with a readily available source of fuel. In one scenario, the host might be capable of acetic fermentation. During which, sugars are broken down into pyruvate which is later decarboxylated and converted into acetyl CoA. Afterwards, the acetyl CoA can be used to produce Acetyl phosphate which is later used to phosphorylate an ADP molecule, thereby producing ATP and acetate.
This process is incredibly ancient and may go as far back as LUCA, so it's likely to develop readily throughout the universe. Additionally, acetic acid bacteria are incredibly successful and already form a ton of close associations with methanogens, so there is precedent for an endosymbiotic merger developing between the two.
(Above) Here's a quick doodle depicting an endosymbiotic relationship between a facultative aerobe / acetate fermenter and an acetolactic methanogen. The end result of this partnership is 2 net ATP from glycolysis (the conversion of sugars to pyruvate), 1 ATP from the breakdown of acetyl phosphate, and an additional 2 ATP for every mol of acetate used up in methanogenesis.
In short, a methanogen could serve as the basis of energy production for a eukaryote-like organism, but its evolutionary avenues would be somewhat impeded upon by nutritive requirements, substrate availability, and low energy conversion efficiency during respiration. However, a relationship between an acetate fermenter and a methanogen could resolve the problem of acquiring substrates.
Sidenote : In researching this topic, I realized that hydrogenosomes (highly-derived mitochondria that allow eukaryotes to survive in anaerobic habitats) produce similar amounts of ATP to methanogens; averaging at around 1 mol of ATP per every mol of substrate. As a result, these organisms might provide us with a window into how methano-eukaryotes might develop. However, its important to keep in mind that these organisms are restricted primarily to anoxic sediments, which would greatly curb their evolutionary avenues (animal and plant analogues aren't likely to develop under meters of marine sediment or within the guts of termites).
(Above) A random assortment of anaerobic protists
that are reliant upon hydrogenosomes for ATP.
DISCLAIMER : feel free to use this idea in your own work, but be sure to provide credit. Additionally, I should note that this might make its way into a future project of mine as well.
Citations :
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289024/#:~:text=Depending%20on%20the%20substrates%2C%20methanogens,such%20that%20the%20overall%20Gibbs'
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0020453
https://www.sciencedirect.com/topics/medicine-and-dentistry/hydrogenosome#:~:text=1%20ATP%20is%20generated%20per,Succ.%2C%20succinate%3B%20Succ.
A video of some anaerobic ciliates collected from the digestive tracts of termites : https://www.youtube.com/watch?v=dLAdNOQCiik
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