Talmudic Question #23

Methanogenesis is characteristic of Archaea (and, according to some, plants as well). Why don't bacteria make methane? (Courtesy of David Lipson).

Comments

[david lipson]

(regarding Bill Martin's comment):I think the only coherant response I have is that, so far, the most extreme hyperthermophiles are all Archaea - bacteria can't do better than about 90oC, Archaea have been grown in the lab up to about 121oC.

[bill martin]

(regarding David Lipson's comment) If tetraether lipids are essential to life in extreme enviroments (his comment) then how and why do eubacteria survive in extreme environments. A Talmudic question -- but only if you believe that tetraethers are the entry password to the extreme. If not, no Talmud needed there (but it always helps, I admit, as someone who cannot read Hebrew.)

[David Lipson]

As I am partly to blame for starting this thread (via Elio’s prodding for interesting, unanswerable questions), I will try to contribute my ecological perspective on this argument. The explanation as to why only Archaea produce methane inevitably seems to come down to it being a historical, evolutionary fluke: Archaea first developed the trait, and have managed to hold on to that niche. However, I think the postings by Bill Martin and SMC point out that it was a very deep, ancient and fundamental fluke – a divergence in the early evolution of life. The suggestion that the earliest form of metabolism on earth was the autotrophic reduction of CO2 using H2 is appealing. Bacteria and Archaea each developed their own solutions to the problem of how to do this, acetogenesis and methanogenesis. Methanogenesis is pretty much the lowest rung on the thermodynamic ladder, so the question then becomes why did both pathways survive, given that they potentially compete? SMC suggests that Archaea preferentially survived in extreme environments (thanks presumably to their tetraether lipids). But there is also an ecological explanation for how methanogens and anaerobic bacteria coexist. The methanogenic niche avoids competition to a large extent with anaerobic bacteria. While it is true that methanogenesis is inhibited in the presence of alternative electron acceptors, coexistence is possible at low pE when only CO2 is available. This is mainly true because of acetoclastic methane production. Even if acetogens outcompete autotrophic methanogens for H2, their end-product, acetate, can be used for methane formation. This becomes a synergism rather than a competition. Similarly, syntrophic bacteria that produce acetate and H2 benefit from the scavenging of their end-products by methanogens. So methanogens have worked out a nice deal with fermentative and acetogenic bacteria. If we accept that autotrophic CO2 reduction was the primordial pathway, it may well have been evolutionary pressure from acetogens (along with the niche they provided in the form of available acetate) that lead to the acetoclastic methanogenesis pathway, which accounts for the majority of contemporary methane production. We don’t often observe direct competition in nature, because usually in competition, someone loses. We mainly see the after-effects of competition manifesting as niche differentiation, such as these tidy little synergisms.

So why don’t bacteria make methane? Why should they? Thermodynamically, it’s a terrible lifestyle. Better to make acetate and leave it to the acetoclastic methanogens to clean up your mess.

[Bill Martin]

The question is very similar to the question that caused me to write a gutwrenching paper not too long ago. The paper was [1]:

The question was: How is it possible that methanogens require help from chemiosmosis in order to generate a proton gradient? Related: why don't they make acetate from H2 and CO2?

One thing leads to another and it doesn't take long before one is staring at the biochemical similarities in the methyl synthesis branch of the acetyl-CoA pathway between acetogens and methanogens and the differences in their proton pumping mechanisms (in the absence of shared proteins before we get to CODH/ACS). As far as I can tell (and I might be wrong, but give me a fair shake and read the paper first, please), there is homology (yes, similar via common descent) between the synthesis of methane and acetate at some hydrothermal vents and the chemistry of the acetyl-CoA pathway as it is manifest in acetogens and methanogens. That might sound nutty, but in the absence of a better suggestion for the main reaction that got life going, I'd say CO2 reduction with electrons from H2 is a pretty good null hypothesis. Sepentinization is a nice key word here, because it is the source of (n.b.) geological H2 and methane (and other reduced C1 compounds) at vents even today. Why should that have been different at life's origin? I suppose that heterotrophic origins first fans will scoff, but that's fine, as long as they can offer a better suggestion for a thermodynamically favourable core reaction (main waste product) at lifes origin that does not require miracles. So I'd say acetate first because its kinetically easy, methane later, because its harder to make. But when I say methane later, I mean methanogenesis as the core phsyiology of the common ancestor of archeabacteria, that descended from a Last Common Ancestor that was not free living. Those who start with a free-living Last Common Ancestor might want to let us know what its lifestyle was supposed to have been. Early evolution is a miserable topic, but I didn't pose the question of this discussion.

Afetr all: the ability to harness a naturally pre-existing proton gradient (at the vent–ocean interface) via an ATPase has to be older than the ability to generate a proton gradient with chemistry that is specified by genes. And if we look around, that tends to fit with what we see in the organisation of modern microbial physiology.

So my answer is: They never learned how, and those that might have made steps in that direction (via LGT or whatever) found themselves unable to compete with preexisting well-honed archaeal competitors that could do it better on the molecule for molecule sucstrate competition basis. The proton pumping mechanisms that enable acetogens and methanogens to work seem to be their own specific solutions to the problem of how to pump your own protons and thus make the transition to the free-living state. Sound crazy? Articulate a better suggestion than in [1].

[1] Martin W, Russell MJ: On the origin of biochemistry at an alkaline hydrothermal vent. Phil. Trans Roy. Soc. Lond. B 367:1187–1925 (2007).

[John Trawick]

SMC's and Paul Orwin's speculations on detoxifying C-1 compounds seem very reasonable; both eubacteria and eukaryotes have non-methane generating systems to perform that function.
Also, reading about the necessary enzyme for methane generation, methyl coenzyme m reductase, it appears that this requires nickel bound to a unique cofactor, coenzyme F430. Biosynthesis of this coenzyme would require multiple steps (and genes). Methyl coenzyme m reductase is strictly anaerobic and it seems possible that this is the only enzyme to directly produce methane. If something selected against horizontal transfer of the needed genes or against some kind of endosymbiotic event, maybe convergent evolution of methanogenesis would be unlikely because Archaea would have a competitive advantage in that environmental niche?

[Paul Orwin]

After reading SMC's interesting story and poking around a bit (read, procrastinating) I think I can maybe add to his hypothesis. The phylogenetic restriction of methanogenesis suggests an ancient origin and restriction (duh!). So, we can think a bit about the Archaeal atmosphere, and a hot, wet, reducing, anoxic world. This seems like a world in which H2 is a pretty robust electron source, so bacteria that can get those will have some success. I'm not sure about CO2 levels in geologically ancient atmospheres, waters, and sediments, but lets assume there was some- This niche seems reasonable to fill at or near the outset.

So, the question becomes what kept these organisms from diversifying their metabolism over evolutionary time (i.e. why are they still methanogens fixing CO2 and getting e from H2 when there are so many other metabolic pathways out there?).

Here's my goofy idea - maybe the intermediates of methanogenic electron transfer and carbon assimilation poison other metabolic pathways. Or, alternatively, other essential parts of the methanogenic cell are incompatible with other chemotrophic energy? This seems a stretch. Alternatively, maybe we just aren't good enough investigating methanogens to know all their metabolic capabilities.

The flip side is why hasn't anyone else developed methanogenesis (which was actually the question!). I have to think that this suggests that the intermediates of methanogenesis poison other metabolic strategies in some way (note, not a biochemist!!), making it an all or nothing proposition. It was noted by SMC that methylotrophy and methanogenesis share some intermediate steps, so maybe those ones are ok, but some critical step is inaccessible to an organism using ROC for energy and cell carbon? An added mystery is that there are lots of H2 utilizing CO2 fixing eubacteria, but they don't make methane (at least, if they do no one is talking about it!).

So (stream of conciousness alert!) maybe that explains it - in eubacteria, an alternative set of tools developed for the same purpose (getting e and carbon), making methanogenesis less attractive

[Paul Orwin]

I've been mulling this over in my addled little brain, and I just don't even have a germ of an idea (sorry!). I guess it could be phylogenetic (the mechanism evolved once after the divergence of bacteria and archaea from their last common ancestor), or maybe it evolved in a reducing atmosphere (they are all obligate anaerobes, right?), and was lost from the bacterial lineage? It doesn't seem like there is a good explanation from first principles. But I'm sure someone can come up with a good explanation that I can't think of!

[SMC]

I am filled with shame.
My amazing wiseass powers have let me down. I thought for sure I'd be able to find at least ONE mention of a methanogenic bacterium somewhere.

FAIL.

In my defense, I hadn't even looked at methanogenesis or methano/methylotrophy until this came up, which also means you're all invited to point and laugh at the admitted ignorance which may be evident in the rest of my answer here...

My best guess (and that's all it is) is that it's sort of a case of evolutionary desperation that some archaea developed the capability. The capability seems to have developed from some functions common to both some archaea and some eubacteria but only some archaea ended up managing to hang on in a fringe environment long enough for the population to develop the ability.

In general, it seems like archaea are largely shoved out into the environmental margins these days, while bacteria dominate around what we freakish eukaryotes think of as "normal" environmental conditions. It is a virtual certainty that bacteria and archaea derive from a common ancestor. I've also often seen it suggested that the sort of extreme environments still dominated by archaea (specifically high temperature and possibly high-pressure environments) represent a likely original environment in which cellular life first arose.

The methane-producing and methane-"eating" biochemical pathways seem to overlap quite a bit - several of the same enzymes are apparently involved in both processes, and it seems like several of them can have more than one "purpose". Though I've seen suggestions that the shared enzymes' genes were the result of horizontal gene transfer, my (again, admittedly inexpert and from a mere undergraduate) opinion is that it is more likely that the shared genes were present in some form in the last common ancestor of both modern-day archaea and eubacteria.

I stumbled on an interesting paper[1] as I was poking around that reports versions of several of these genes were found in the comparatively bizarre bacterial phylum of Planctomycetes. Fascinatingly, the gene sequences in the Planctomycetes examined appear (it is reported) to be about equally evolutionarily distant from both the known methane-eating proteobacteria and the methane-belching archaea. Makes me wonder if perhaps the Planctomycetes might harbor the largest remaining collection (in one group of organisms) of genetic features possessed by the last common ancestor of the eubacteria and archaea - I haven't got the background to make any kind of judgement on whether there's even grounds to speculate about that, but the possibility is really spiffy anyway, as far as I'm concerned.

In any case, here's my perhaps-laughably speculative hypothesis:
We start with the Last Common Ancestor, who had what I'd guess were genes involved in detoxifying "C-1" organic molecules (which might have more than one carbon, but no carbon-carbon bonds e.g. dimethyl ether) like formaldehyde. At some point, we get an evolutionary split. Eubacteria develop features that let them go nuts outside of the original hot environment, while archaea initially end up largely retaining the higher-temperature survival capabilities and are more firmly established there. In the process of all of this, eubacteria perhaps tended to lose much of their former capabilities through evolutionary atrophy (genes that are no longer used are allowed to break over time through natural mutation and eventually end up spliced out altogether in many cases). Archaea do eventually move out from hot/high-pressure environments, but seem to be out-competed in more moderate environments. Still they manage to make their way out to niches that the eubacteria for whatever reason don't bother with, like places with extremely high osmotic pressure (e.g. saturated brines, like the northern end of the Great Salt Lake in Utah). Eventually, some populations of archaea end up in places where there isn't much to dump leftover electrons from metabolism onto except for carbon dioxide, and which perhaps is too hot, or too high a pressure, or whatever for existing eubacteria to tolerate. The archaeal population manages to hang on long enough for some members to develop mutant enzymes which can harness the feeble electron-sucking power of single-carbon molecules and are able to eke out a meager living. Eventually they make their way back out of this tiny niche into other areas which are not as extreme, but now the populations have the ability to continue their metabolic activity by methane production in desperate, electron-acceptor-poor environments where nothing else survives. Both archaea and eubacteria appear to have developed methanotrophy, if I remember what I was looking at over the weekend correctly, so maybe this was spurred on around the periphery of methanogenic archaeal populations by all the new methane being produced.

I've been trying to turn that into a coherent and interesting story off and on all weekend, and this is the best I've managed to do so far. I haven't had much background in this area so helpful comments are appreciated. I did skim over everything pretty quickly and I'd be surprised if I didn't at least miss a few things if not outright misinterpret something...

Incidentally, it appears that ASM's "Microbe" magazine has an overview of the subject available online, too.[2]

[1] Chistoserdova, L., C. Jenkins, M. Kalyuzhnaya, C. J. Marx, A. Lapidus, J. A. Vorholt, J. T. Staley, and M. E. Lidstrom: "The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy." 2004; Mol. Biol. Evol. 21:1234-1241.

[2] Ludmila Chistoserdova, Marina G. Kalyuzhnaya, and Mary E. Lidstrom: "C1-Transfer Modules: from Genomics to Ecology" http://www.asm.org/microbe/index.asp?bid=38603 (retrieved 20071105)

[stan zahler]

I've often wondered about that too. I'm surprised nobody has nade a reasibable suggestion. The only simple-minded thought I've evr come up with is: maybe the difference in cell walls is responsible. Some precursor escapes, or methane can't get out, or . .
At least it's a start of a guess.