Moselio Schaechter


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April 26, 2010

True or False: All Metazoans Need O2

by Elio

I am the Lorax, and I'll yell and I'll shout for the fine things on earth that are on their way out!
                                                                                                                  Dr. Seuss

Loricifera

A loriciferan from L’Atalante Basin. Scale
bar: 50 mµ. Source.

Life without air—a term coined by Louis Pasteur, the discoverer of anaerobiosis—has been thought to be exclusively a property of microbes, be they prokaryotic or eukaryotic. Multicellular organisms were thought to lack this talent. Until recently that is, when an Italian and Danish group led by Roberto Danovaro looked at an unusual-sounding habitat, a brine “lake” at the bottom of the Mediterranean, nearly 200 km from Crete. Called L’Atalante Basin, this area was formed when salt dissolved from the sea’s subsurface and accumulated in underwater depressions. Eight times more saline than seawater, this layer does not mix with the water column above it and, like the underlying sediment, is completely anoxic. This particular site is not unique; so-called oxygen minimum zones are found in all the oceans at fairly shallow depths as such things go, usually from 200 m to 1,500 m. Characteristically, they have very low available oxygen and lots of sulfide.

Extremophilic archaea and bacteria are common in such inhospitable-sounding environments, and so are a few eukaryotic microbes, notably protozoa. The news is that one can also find small multicellular living animals at this site. These include members of the Loricifera, metazoans less than a millimeter in length that are common inhabitants of the more usual marine sediments. Their name, sounding like something from Dr. Seuss, actually stems from their exoskeleton that serves as armor (lorica in Latin). Loriciferans have been found in hypersaline marine sites before, but they were presumed to be remnants of dead organisms falling from above (the “rain of cadavers”). However, although they are abundant in the anoxic zone, in the last 40 years only two specimens had been found in the deep Mediterranean Sea above it. This new report shows that these little animals are actually alive, as demonstrated by their life-like morphology, their uptake of radioactive leucine, and their staining with “vital” dyes. Some had eggs in them. Other kinds of metazoans in the same samples were clearly dead.

So, how do these anaerobic loriciferans harvest their energy?

Hydrogenosome

A hydrogenosome-like body in a
section of a loriciferan. Source.

Not much is known about this at present, but transmission electron microscopy of thin sections shows that they lack mitochondria and possess vesicular structures that resemble hydrogenosomes. Hydrogenosomes have been seen in various unrelated unicellular anaerobic eukaryotes, such as trichomonads, ciliates, chytrid fungi, and heterolobosean flagellates. They had never been previously observed in multicellular organisms, so this itself would be news. To remind you, hydrogenosomes produce energy by converting pyruvate into acetate and CO2, releasing hydrogen in the process. These structures are thought to be derived from mitochondria. However, with the exception of the cockroach-gut inhabiting ciliate Nyctotherus ovalis, hydrogenosomes are not known to contain DNA. All cells so far have been found to host either mitochondria or hydrogenosomes, never both. (May I ask a question? Does the energy metabolism of hydrogenosomes qualify as anaerobic respiration?) Right now, it’s too early to tell the nature and source of these organisms’ electron donors and acceptors. Do they oxidize the abundant H2S? Do they reduce sulfate or something else? Surely, answers to these questions will be soon forthcoming.

Metab_nature

Hydrogenosomal metabolism in Trichomonas vaginalis. Enzymes
are indicated as follows: 1, pyruvate:ferredoxin oxidoreductase;
2, NAD-dependent malate dehydrogenase (decarboxylating); 3,
NADH:ferredoxin oxidoreductase activity of the 51-kDa (Tvh-47)
and 24-kDa (Tvh-22) catalytic flavoprotein component of complex
I; 4, ferredoxin-dependent Fe-hydrogenase; 5, hypothetical NAD-
dependent 65-kDa Fe-hydrogenase; 6, acetate:succinate CoA-trans-
ferase; 7, succinate thiokinase. Source.

But before even worrying about energy metabolism, one should ask, what do these organisms eat? A likely menu being bacteria and archaea, there not being much else where they live (although falling cadavers might be also a source of food). Other loriciferans have a complicated set of protrusions that are often seen covered with bacteria. Also, their digestive tract is often filled with partly digested prokaryotic cells.

Are there other metazoans living in yet other anaerobic environments? The present finding strongly suggests that it’s worthwhile looking with fresh eyes in such habitats. Who knows what one will find. But clearly we have here another instance of an exception to the rule, something that Biology seems to be full of.

ResearchBlogging.org

Danovaro R, Dell'anno A, Pusceddu A, Gambi C, Heiner I, & Møbjerg Kristensen R (2010). The first metazoa living in permanently anoxic conditions. BMC biology, 8 PMID: 20370908

Comments

I think there may be a difference between occasional anaerobiosis and the permanent one of these creatures.

This truly is an amazing find! However, when looking through their paper, it appears that their only argument for the mystery organelles being hydrogenosomes is that they, um, "look" like hydrogenosomes.http://www.panbeadsstore.com/pandora-chains/pandora-gold-chain-w18.html

One question that might be asked is where do these anaerobic metazoans obtain cellular components that require oxygen for synthesis? Membrane sterols and unsaturated fatty acids in eukaryotes each have an O2-requiring step in their biosynthetic pathways.
Presumably, like some other eukaryotes, they could acquire sterols and UFA from food--eating the detritus that falls down into their anaerobic domain.

Fascinating! Many thanks for enlightening us.

Elio

Elio! I am compelled to point out not one, but two striking similarities between the Lorax and yourself. First, and most importantly, you both speak passionately on behalf of those who "have no tongues" (in your case, the Small Things, for The Lorax, the Truffula Trees). Second, well... anyone who is interested can Google image results for "Lorax" and compare them with picture at the top of this page. Or try http://en.wikipedia.org/wiki/The_Lorax

Welkin,
Is the second good or bad?
Elio

I'm mystified. I had been given to understand that cnidarians, and even many fish, happily switch to anoxic metabolism when they find themselves without. Is the surprise that lociferans can even reproduce without oxygen?

I think there may be a difference between occasional anaerobiosis and the permanent one of these creatures.

Elio

Correction: To be fair, the authors wrote hydrogenosome-LIKE organelles; everyone else seems to have ditched the -like part and gone along with the hydrogenosome story...

It's hard to find fault with your statements. I also believe that they could have firmed up the argument for or against hydrogenosomes, with relatively little effort. I imagine that such experiments are under way. Anyhow, I;m glad that you agree that this is an interesting and potentially very important piece of work.

Elio

This truly is an amazing find! However, when looking through their paper, it appears that their only argument for the mystery organelles being hydrogenosomes is that they, um, "look" like hydrogenosomes. There's a few people in our department who'd have a fit about that, as not only could those blobs technically be -anything-, but not all reduced mitochondria are hydrogenosomes -- there are also plenty of mitosomes (eg. as in microsporidia) and mitochondria-like-organelles (MLOs) that represent varying degrees of mitochondrial reduction, and do not synthesise H2. There's a nice paper discussing various reduced mitochondria by Stechmann et al. 2008 Curr Biol here: http://ukpmc.ac.uk/articlerender.cgi?accid=pmcA2428068 (hopefully free access)

I would've expected them to do some basic staining (eg. MitoTracker should probably work) at the very least before they claim those organelles are mitochondrial-derived, and would've hoped for some biochemical analyses prior to claiming those as hydrogenosomes specifically. Also, hydrogenosomes tend to attract endosymbiotic methanogens in the parabasalian examples, so one could make some guesses by identifying the reported bacterial endosymbionts, although that would still be quite sketchy.

Basically, I'm kind of annoyed they jumped to the conclusion those are hydrogenosomes without really having investigated that matter properly, and that the scientific community hasn't really bothered to tread as carefully as we should...

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