Ovobac­ter pro­pel­lens, Not Your Av­er­age Bor­ing Bac­terium

by Elio

I bet most of you have never heard of this one. And you are not alone in this. Look for it by name in PubMed and you find two en­tries, both from the same lab. This bug de­serves bet­ter. Found by us­ing a fairly di­rect en­rich­ment tech­nique from sed­i­ments in shal­low Dan­ish wa­ters, this or­gan­ism evinces as­pects of both struc­tural and phys­i­o­log­i­cal unique­ness. It is seen as an ovoid cell that looks less like a bac­terium than like a small cil­i­ate. The ev­i­dence that it is a prokary­ote re­lies on mor­phol­ogy alone, as it has not been cul­ti­vated nor has its DNA been se­quenced.

TEM sec­tion through an O. pro­pel­lens show­ing the abun­dant fla­gella and a row of reg­u­larly spaced, elec­tron dense or­ganelles con­sist­ing of stacked mem­branes. Bar = 1 μm. Source

Ovobac­ter pro­pel­lens (or, to re­luc­tantly obey one of my least fa­vorite rules of tax­on­omy, Can­di­da­tus O. pro­pel­lens) ap­pears as large ovoid cells, 4–5 μm in length, each pos­sess­ing a huge tuft made up of some 400 fla­gella. Armed with such equip­ment, it trav­els at as­tound­ing speeds, hav­ing been clocked at 1 mm per sec­ond. (That's some 200 body lengths. To equal that, a hu­man would have to swim at over 300 me­ters per sec­ond.) Now for a small di­gres­sion: by chance I en­coun­tered a most in­for­ma­tive ta­ble of ex­am­ples of mi­cro­bial motil­ity. You will no­tice (see ta­ble) that while para­me­cia outswim all oth­ers in terms of ve­loc­ity, pro­tists and bac­te­ria alike, O. pro­pel­lens matches them.

So, what makes this or­gan­ism a prokary­ote? DAPI stain­ing shows that its DNA is cer­tainly not con­tained in a nu­cleus. In­stead, it is con­cen­trated at the pe­riph­ery of the cell, in a cy­to­plasm that sur­rounds a large vac­uole. Thin EM sec­tions show that its fla­gella ap­pear rooted in a de­pres­sion on one side of the cell. Be­low this is a row of 12–13 box-like elec­tron-dense or­ganelles made up of stacked mem­branes. The func­tion of this un­usual struc­ture can only be guessed at. Fur­ther­more, in sec­tions one can see a Gram-neg­a­tive-like dou­ble mem­brane. But the or­gan­isms re­veal other mor­pho­log­i­cal pe­cu­liar­i­ties, in­clud­ing in­tra­cel­lu­lar mem­brane chan­nels, for de­tails of which I ask read­ers to con­sult the orig­i­nal pa­per.

Schematic of the struc­ture of Ovobac­ter pro­pel­lens. (Above) Trans­verse sec­tion (''ven­tral'' side to the left). (Be­low) The cell seen from the ''ven­tral side'' (with the right end of the cell turn­ing to the left in the fig­ure). sm = stacked mem­branes; mb = mem­brane band. Bar = 1 μm. Source

The cells swim freely and do not ap­pear to at­tach to sur­faces. Be­cause the fla­gel­lar tuft is not aligned with the ma­jor axis of the cell, the coun­ter­clock­wise ro­ta­tion of the tuft re­sults in the cells them­selves ro­tat­ing clock­wise. Con­se­quently the cells do not swim in a straight line, but rather along a he­li­cal path. In­ter­est­ingly, when these cells change di­rec­tion, they do not tum­ble, as is usual for fla­gel­lar motil­ity. Just how they do it is not clear. For re­views on fla­gel­lar motil­ity, click here and here.
 

When these cells reach their de­sired oxy­gen con­cen­tra­tion, be­tween 0 and 1% of at­mos­pheric sat­u­ra­tion, they move at ran­dom within a nar­row band (typ­i­cally 150 μm wide). Since the or­gan­isms have not been cul­ti­vated, it's hard to know what sub­strate they pre­fer for ox­i­da­tion. There are no signs of sul­fur or iron in­clu­sions, as would be ex­pected from sul­fide or fer­rous iron ox­i­da­tion, so the ba­sics of its en­ergy me­tab­o­lism await to be elu­ci­dated.

a Di­a­gram of O. pro­pel­lens swim­ming. The fla­gel­lar tuft ro­tates counter-clock­wise, mak­ing the cell ro­tate clock­wise. The ve­loc­ity vec­tor (large ar­row) is not aligned with the ro­ta­tional axis, which re­sults in a he­li­cal swim­ming pat­tern. b Ovobac­ter swim­ming. (Above) Its he­li­cal path. (Be­low) High-speed video record­ing. The time in­ter­val be­tween dots is 1.5 ms. Bar = 5 μm. Source

With re­gard to their un­usual speed, the au­thors make the point that, for most bac­te­ria, swim­ming is not a good way to boost their up­take of dis­solved sub­strates, the speed of dif­fu­sion into the cell be­ing greater than that of cell move­ment. How­ever, the large size of Ovobac­ter and its amaz­ing speed of move­ment may open this up as a pos­si­bil­ity. The pa­per in­cludes some cal­cu­la­tions of (I quote) the Peclet num­ber (also named Sher­wood num­ber): Pe = L x v/D, where L is length, m is swim­ming ve­loc­ity and D is the dif­fu­sion co­ef­fi­cient. If Pe > 1 then ad­vec­tive trans­port may be sig­nif­i­cant. The value of D is about 2 x 10^-15 cm² s^-1 for dis­solved O₂ and if we as­sume a cell length of 4x10^-4 cm and a swim­ming ve­loc­ity of 0.07 cm s^-1, we have Pe = 1.4 and so some im­por­tance in terms of up­take of solutes can­not be ruled out. Sounds mar­ginal but plau­si­ble.

Ovobac­ter is en­dowed with a num­ber of un­ex­pected prop­er­ties whose sig­nif­i­cance, by and large, await fur­ther in­ves­ti­ga­tion. It seems a pity that work with this fas­ci­nat­ing or­gan­ism does not ap­pear to have been fol­lowed up. But the gen­eral les­son is that the world's mi­cro­biome is end­lessly full of sur­prises.

Hot off the Press: A new ar­ti­cle in Ap­plied and En­vi­ron­men­tal Mi­cro­bi­ol­ogy re­ports that some ar­chaea can com­pete for be­ing the fastest swim­mers with Ovobac­ter. Methanocal­do­coc­cus jan­naschii and M. vil­lo­sus were clocked at 400–500 body lengths/second. How­ever, be­ing smaller, their speed is ac­tu­ally around 300 μm/second, which is about one third of that of the larger Ovobac­ter. So, it de­pends how you mea­sure speed.

Ref­er­ence

Fenchel T, Thar R (2004). "Can­di­da­tus Ovobac­ter pro­pel­lens": a large con­spic­u­ous prokary­ote with an un­usual motil­ity be­hav­iour. FEMS Mi­cro­bi­ol­ogy Ecol­ogy, 48 (2), 231−238. PMID 19712406