Methanogenesis is among the most energy-dense forms of anaerobic respiration. Typically, it requires the environmental presence of hydrogen to reduce CO2; however, hydrogen can be generated from glucose in hydrogenic fermentation, which also produces some metabolic energy.

So, suppose we have an anoxic world where the animal-equivalents breathe in carbon dioxide instead of oxygen, exhale methane, and produce acetate, glyoxylate, and formate (and possibly traces of a variety of other light organic compounds) as additional metabolic wastes; effectively, carbon waste ends up having to be excreted in (the equivalent of) urine a byproduct of normal energy-producing metabolism, parallel to the excretion of nitrogenous wastes from the catabolism of proteins and nucleic acids.

Given that oxygenic phototsynthesis must be suppressed (if it exists at all, it at least must be uncommon, 'cause the whole point is that we want animals to breathe CO2, not oxygen), what does the rest of the ecosystem look like, in terms of basic anabolic / catabolic processes? In particular, what are plants doing, given that CO2 is abundant, methane reasonably common in the air, and animals are pumping out tons of other simple organics along with the methane?

Edit: For reference, the net reactions for acetogenic, glyoxylogenic and formogenic catabolism of glucose are as follows:

$C_6H_{12}O_6 → 2CHCO_2O^- + 2H^+ + 2CH_4$ Glucose ferments into glyoxylate and 2 methanes.

$2C_6H_{12}O_6 + 2H_2O + CO2 → 4CH_3COO^- + 4HCOO^- + 8H^+ + CH4$ Glucose is hydrolyzed and oxidized by carbon dioxide to produce 4 acetates, 4 formates, and methane.

Note that the glyoxylogenic reaction actually doesn't consume CO2--only the mixed-acid acetate / formate pathway; this is because the CO2 used in the glyoxylate pathway is actually endogenously generated during the initial breakdown of glucose via pyruvate. That pathway would be the equivalent of our anaerobic respiration. Both pathways hide a bunch of complexity where hydrogen and sometimes endogenous carbon dioxide are generated along the way, before eventually all of the hydrogen is used up creating various small organics.

  • $\begingroup$ Well, in the real history of life what plant did was pollute the environment with oxygen; the oxygen was initially soaked up by the available iron (leading to the massive iron oxide deposits which we have been exploiting for thousands of years barely making a dent). When the available iron was exhausted the oxygen pollution lead to the extinction of the pre-oxygenation ecosystem. $\endgroup$ – AlexP Sep 1 '19 at 19:37

In particular, what are plants doing, given that CO2 is abundant, methane reasonably common in the air, and animals are pumping out tons of other simple organics along with the methane?

If one thing is sure, you can't have plants in such ecosystem.

Plant as we know them expel oxygen as byproduct of photosynthesis, and as you state

oxygenic phototsynthesis must be suppressed

If there is any photosynthetizer, it would probably follow the inverse path of methanogenyc respiration instead of

CO2 + 4 H2 → CH4 + 2 H2O + Energy

they would do something along the line of

CH4 + 2 H2O + Energy → CO2 + 4 H2

To store the species so synthesized the pluricellular organisms would need bags (Earth plants produce sugars, which are solid and easier to store), which would make them appear like large bubbles.

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  • $\begingroup$ If your photosynthesizers aren't producing an sugars, then what are the animals eating? And what happens to all of the organic wastes that animals are expelling? $\endgroup$ – Logan R. Kearsley Sep 1 '19 at 23:41

You have flipped the scenario currently in the sunny topside of earth.

Here, animals breathe O2 and use it to oxidize the reduced carbon fixed by plants. The animals breathe out CO2 and hydrogen (as H2O).

Plants scrounge up scarce CO2 and with hydrogen (obtained as H2O) , use the energy of the sun to fix it back into reduced carbon, as carbohydrates.

Flipping this in your scenario, your animals take in CO2 and hydrogen and expel reduced carbon as methane. "Plants" (considered as primary producers) will presumably take up the reduced carbon as methane, scrounge up scarce O2 and use some ambient energy to reform the CO2. Nice that the reduced carbon here is methane; if you are a plant there are better odds of CH4 drifting into your vicinity than glucose.

In your scenario the reduced carbon is methane; in ours we generally eat carbohydrates. It is all reduced carbon.

I think the trick is how much O2 is available. Prevalence of O2 will tip the balance one way or the other, as it presumably did in the early earth and still does in anaerobic / microaerobic environments.

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EDIT: After looking more into the energetics, CO2-breathing probably won't work with glucose as an energy storage molecule. Some other energy-storage system that has more hydrogens available to liberate may still allow CO2 breathing, but if we stick with glucose, a methanogenic biosphere ends up quite different.

It turns out that decomposing an/or reducing acetic acid is actually more efficient than reducing carbon dioxide... so glucose-eating animals using hydrogenic fermentation would not need to breathe CO2 after all. Cf.:

Acetoclasis: $C_2H_4O_2 → CO_2 + CH_4 + 28 kJ/mol$

CO2 reduction: $CO_2 + 4H_2 → 2 H_2O + CH_4 + 17.4kJ/mol H_2$

In fact, CO2 reduction is the very last phase of methanogenesis in terrestrial decomposition, after all other organic substrates are consumed.

Instead, you get a purely-fermentative metabolism that ends up shuffling hydrogens around internally, after some water-consuming hydrolysis reactions, to produce formic acid and methane. The high-level reactions are as follows:

Glycolysis: $C_6H_{12}O_6 → 2 C_3H_4O_3 + 4H$

Pyruvate cleavage: $C_3H_4O_3 + 2 H_2O → C_2H_4O_2 + H_2CO_2$

Acetic acid reduction: $C_2H_4O_2 + 2H → H_2CO_2 + CH_4$

with the final fermentation products being 4 formic acids and 2 methanes.

Meanwhile, "plants" can construct glucose directly from methane and carbon dioxide, but only the methane gets regenerated by animals. So, rather than an oxygen crisis, this world ends up with an acidification crisis as CO2 and water are used up and replaced by formic acid and even more methane, and plants have to switch over to consuming formic acid instead of CO2 (via the reaction $2 H_2CO_2 + CH_4 → C_3H_4O_3 + H_2O + 2H$, followed by re-assembly of pyruvate into glucose) and producing water as a byproduct of photosynthesis. In our world, bacteria use up energy to selectively decompose formic acid into CO2 and hydrogen to control pH, so that might limit the extent of an acidification crisis... but it would be a thing that sessile autotrophs "waste" energy on to ensure their survival, not something animals would bother doing most of the time... although replacing acetic acid reduction with acetoclasis (resulting in excess hydrogen production) in high-exertion situations where there isn't time for proper acid waste disposal might result in some atmospheric hydrogen buildup. On a small world, that would probably eventually lead to a much-delayed mass-extinction-causing oxygenation event as hydrogen is lost to space, but on a larger world it might result in the eventual conversion over to a more "traditional" hydrogen-breather ecology.

Original Answer: Alright, having contemplated this some more myself, here's what I've come up with:

Glyoxylogenic fermentation can be pretty much ignored. It's a red herring. Insofar as how it interacts with the broad autotroph/heterotroph cycle, it's analogous to lactate-producing anaerobic respiration on Earth; it's a stop-gap method of energy production, and when oxidizers become available again, glyoxylate will get cleaned up through a variety of further reactions.

If we start out with a world in which both CO2 and methane are reasonable abundant, then building glucose from those materials is really cheap ($3CO_2 + 3CH_4 → C_6H_{12}O_6$). That should allow rapid autotrophic growth, limited only by availability of other essential nutrients, which will pull gasses out of the atmosphere until either CO2 or methane become a limiting factor.

If we suppose that methane is the limiting factor, then there will still be lots of primordial CO2 still floating around that can be used in the proposed methanogenic respiration pathways to oxidize glucose. This world will therefore never have the equivalent of the "oxygen catastrophe". What advanced animals breathe will be remarkably similar to the original primordial atmosphere.

As heterotrophic life develops, though, the environment will instead be flooded with simple organic acids--primarily acetate and formate. That doesn't affect the atmosphere overly much, but it does affect the oceans and the rainfall. Conveniently, acidification can result in the release of even more atmospheric CO2, as carbonate is extracted from minerals; and microbes or fungal-like organisms with access to alternative anions could in fact use up formic and acetic acid as hydrogen sources to produce water, methane, hydrogen sulfide, etc. along with formate and acetate salts.

Much like with our oxygen crisis, though, geological mineral reservoirs capable of absorbing organic acids will eventually run out, and they'll start building up.

With methane levels being kept low by efficient autotroph absorption, eventually it will become more preferable to start using the abundant organic acids as a carbon source instead.

Conventiently, acetic acid (presumably through a complicated serious of intermediate reactions) can be rebuilt into glucose without any net external inputs, through the simple formula:

$3C_2H_4O_2 → C_6H_{12}O_6$

Getting glucose from formic acid is more complicated--it's got too much oxygen in it. It can be broken down in two ways, however, giving water and carbon monoxide, or CO2 and hydrogen:

$CH_2O_2 → CO + H_2O$

$CH_2O_2 → CO_2 + H_2$

Which can be recombined to give formaldehyde, water, and CO2. 6 formaldehyde units ($H_2CO$) form a glucose, so we get the net reaction:

$12CH_2O_2 → C_6H_{12}O_6 + 6H_2O + 6CO_2$

which regenerates atmospheric CO2 for animals to breathe.

So, we end up with a rather complicated cycle in which "plants" consume acetic acid, formic acid, methane, and carbon dioxide to build hydrocarbons, producing water and carbon dioxide as byproducts, while "animals" consume glucose, water, and CO2, and produce acetic acid, formic acid, and methane as byproducts. Note, however, that the consumption of methane by "plants" does not result in the production of extra CO2--rather, they are consumed in a one-to-one ratio. When an "animal" uses up CO2 to oxidize glucose, the methane that results does not go on to be recycled back into CO2--rather, all of the CO2 that animals need is regenerated from their liquid waste formic acid.

Now, although the actual step-wise reactions are more complicated, we can actually separate out the production and consumption of acetic acid as its own independent cycle:

$C_6H_{12}O_6 → 3CH_3COO^- + 3H^+ → C_6H_{12}O_6$

and, like glyoxalate, disregard it when considering how CO2 and methane are exchanged, which provides us with simplified equations to demonstrate how ecological equilibrium is maintained. In the CO2 metabolism, each molecule of glucose is oxidized by a single CO2 in conjunction with hydrolization by 2 waters, producing 1 acetic acid, 4 formic acids, and 1 methane, as follows:

$C_6H_{12}O_6 + 2H_2O + CO2 → CH_3COO^- + 4HCOO^- + 5H^+ + CH4$

As indicates above, it takes 12 formic acids to produce 1 new glucose molecule, so tripling this gives us the following glucose cycle:

$3C_6H_{12}O_6 + 6H_2O + 3CO2 → 3CH_3COO^- + 12HCOO^- + 15H^+ + 3CH4 → 2C_6H_{12}O_6 + 6H_2O + 6CO2 + 3CH4$

Note at the end that the total CO2 production by "plants" during formate-based glucose anabolism is twice as great as methane production by "animals" during methanogenic respiration. Thus, one more step (using the primitive CO2+methane glucose production pathway, eliminating all of the methane) gets us back to the beginning, with an excess of 3 CO2s left in the atmosphere for "animals" to breathe.

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