Archaeal Web

A venting black smoker emitting sulfide-rich
fluids. Courtesy of University of Washington

Deep sea hydrothermal vents are characterized by steep physical and chemical gradients and by the presence of unusual and fascinating life forms. Varied organisms grow there: giant tube worms that exploit the metabolism of sulfide-oxidizing bacteria, clams, crabs, shrimps, and more. These like their water tepid. But some archaea prefer the hotter neighborhood near the vents that emit water at around 400°C. These microbes are hyperthermophiles, thriving at temperatures around 100°C. Many have a specialized life style, and one them, Pyrodictium, is particularly interesting.

SEM of Pyrodictium
occultum cells enmeshed
in their sticky, glycoprotein
matrix. Source: Reinhard
Rachel

First discovered in 1979 by Karl Stetter’s group, these organisms are strictly anaerobic chemoautotrophs that get their energy from oxidizing hydrogen (and reducing elemental sulfur) by this reaction: H₂ + S° → H₂S. Of interest to us here, these archaea associate to form web-like flakes that are visible with the naked eye. Pyrodictiums are flat, irregularly shaped, disk-like cells 0.3 to 2.5 μm across and up to 0.3 μm thick, sometimes thinning out to a mere 0.08 μm thick. Individual cells are enmeshed in a unique, extracellular matrix made up of bundles of hollow tubules, the cannulae (Latin: “little reeds”). Cannulae have an outer diameter of only 25 nm but can be up to 40 mm long. They are built from three (and perhaps more) glycoprotein subunits ordered in a helical array—an architecture that can withstand temperatures up to 135°C without denaturation or loss of secondary structure. Cannulae make up a large portion of the biomass of Pyrodictium cultures, an investment that bespeaks their importance for these organisms.

A reconstruction from an
electron tomographic scan
in false color showing two
cannulae (yellow), one
inside the periplasm (blue)
of a cell (magenta). Source

Growth and division of these organisms was observed at 90°C under anoxic conditions using a dark-field light microscope (which takes quite a set-up). The researchers observed that growth of the cannulae is directly linked to cell division. When the progeny cells separate afterwards, they remain connected by their cannulae. Repetition of this process over and over results in a dense network, with each cell having multiple connections with its neighbors. Using electron tomography, the cannulae were seen to penetrate into the periplasmic space, which looks like a sturdy way to anchor the cells to the cannulae. Thus, each cannula must pass through an outer membrane twice, which seems like a good trick. Is such a thing seen in any other prokaryotic cell?

Why do these archaea go to the trouble to construct such elaborate and expensive structures? Not having tools for genetic studies at hand, one can only guess. But this mechanism must be vitally important; cultures maintained in the laboratory for over 20 years have never produced a cannula-less mutant. Cannulae are hollow, suggesting they may play some role in transport, in addition to creating Pyrodictium's macro-architecture. As is the case with many archaea, these organisms invite many more studies about their innovative way of life.

Comments

[elio schaechter]

Peter,

You are right, and various authors have pointed out that Pyrodictium should be considered to be a multicellular organism. The concept of multicellularity among prokaryotes is gaining momentum.

Elio

[Peter Ellis]

If the cannulae are hollow and transport materials between cells, is it really correct to regard Pyrodictium as a unicellular organism?

[Mark O. Martin]

I was fortunate enough to be a guest in Ken Nealson's lab when some of the very interesting work with electrically conductive nanowires was carried out. Turns out that mutations in the cytochrome genes have the expected effect!

Bretschger, et al. (2007). "Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants." Appl. Environ. Microbiol. 73: 7003 - 7012.

Shewanella is an interesting beast. It can grow at 37 degrees and at 4 degrees. But it hyperpiliates and forms long motile filaments when grown in the cold.

Abboud, et al. "Low-temperature growth of Shewanella oneidensis MR-1." Appl. Environ. Microbiol. 71: 811 - 816.

I love the microbial world. I guess that makes me a micronerd.

[elio schaechter]

Good thought, Mark. Stay tuned. We'll not slight nanowires in this blog.

Elio

[Mark O. Martin]

Perhaps the cannulae can act like the newfangled "nanowires" in the literature, allowing Pyrodictium to pick up or drop off electrons at a great distance from the cell itself. I'm thinking of situations where the "electron depot" would be in the superheated water...

Gorby, et al. (2006). "Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms." PNAS 103: 11358 - 11363.

Reguera, et al. (2005). "Extracellular electron transfer via microbial nanowires." Nature 435: 1098 - 1101.

[Larry Ayers]

Such a fine post, Elio! Concise and full of interesting information about a realm and its organisms which I'll most likely never experience first-hand.