The At­trac­tion of Mag­ne­to­tac­tic Bac­te­ria

by Daniel P. Haeusser

Mo' Force and Mo' Speed for MO‑1

Reg­u­lar read­ers of Small Things Con­sid­ered may re­call our men­tion of the mag­ne­to­tac­tic bac­te­ria, or­gan­isms that can sense the Earth's mag­netic field to ori­ent them­selves and dis­tin­guish up from down. The mag­ne­to­tac­tic bac­te­ria vary greatly in mor­phol­ogy, me­tab­o­lism, and phy­logeny, but they all share a lit­tle tool that per­mits the mag­netic sens­ing un­der­ly­ing their co­or­di­nated move­ment (mag­ne­to­taxis). This tool, the mag­ne­to­some (also dis­cussed here in an ear­lier post) con­sists of mag­netic min­eral in­clu­sions bounded by a lipid bi­layer.

Fig­ure 1. (A) Trans­mis­sion elec­tron mi­cro­graph of uranyl-stained MO‑1 cell with its sheathed fla­gel­lar bun­dles (ar­row­head) along the long hemi­sphere of the cell. Ar­row shows in­di­vid­ual fla­gella at the cell dis­tal end of the sheath. Scale bar = 500 nm. Adapted from: source. (B) Slice from a cryo-elec­tron to­mo­gram show­ing a side view of an in­tact fla­gel­lar ap­pa­ra­tus on the cell en­ve­lope of a vit­ri­fied MO‑1 cell. Black ar­row­heads show where the sheath at­taches to the base plat­form, which has a di­am­e­ter (d0) of 230 nm and a depth (d1) of 46 nm. Yel­low ar­row­heads show three vis­i­ble in­di­vid­ual fla­gella in the sheathed bun­dle in this slice, of the seven to­tal fla­gella. Adapted from: source

As Elio stated in his ear­lier post: "The ac­tual merit in be­ing mag­netic has not yet been set­tled de­fin­i­tively. It has been pro­posed that these bac­te­ria swim along the mag­netic field lines to reach the lower strata of the ma­rine sed­i­ment. That's where the oxy­gen con­cen­tra­tion is very low, some­thing they may like."

A re­cent re­port in En­vi­ron­men­tal Mi­cro­bi­ol­ogy be­gins to look closer into the ad­van­tages of mag­ne­to­taxis for a strain called MO‑1, an iso­late from the Mediter­ranean Sea that rep­re­sents a po­ten­tially novel genus of Pro­teobac­te­ria and is phy­lo­ge­net­i­cally re­lated to Mag­ne­to­coc­cus strains. MO‑1 has an ovoid mor­phol­ogy with two sheathed, fla­gel­lar bun­dles on its long-axis side (Fig­ure 1A), that im­part strong force gen­er­a­tion to achieve MO‑1 speeds up to 300 µm/sec (~100 body-length­s/sec­ond), about ten-fold faster than the av­er­age ma­rine species of bac­te­ria. It re­sem­bles in looks a non-mag­ne­to­tac­tic fast swim­mer, Ovobac­ter pro­pel­lens, dis­cussed in these pages.

En­cas­ing a Flock of Fla­gella

Fig­ure 2: (A) Neg­a­tively stained elec­tron mi­cro­graph of a base plat­form treated in a ba­sic (pH 11) so­lu­tion show­ing an in­ter­twined hexag­o­nal ar­ray (with car­toon over­lay on right) of the basal bod­ies of seven fla­gella (or­ange in car­toon) and twenty-four fib­rils (green in car­toon). Scale bar = 50 nm. Adapted from source. (B) Di­a­gram from 1957 de­pict­ing a sim­i­lar, then newly vi­su­al­ized, dou­ble hexag­o­nal ar­ray of fil­a­ments (now known to be actin and myosin) in cross-stri­ated mus­cle. Adapted from: source

As re­vealed by ge­netic analy­sis and cryo-elec­tron mi­croscopy, these fla­gel­lar bun­dles of MO‑1 make up some amaz­ing struc­tures (Fig­ure 1B). Each bun­dle con­sists of seven fla­gella with twenty-four in­ter­spersed fib­rils (Fig­ure 2A) that are arranged and move against one an­other in a man­ner that re­sem­bles the thick and thin fil­a­ments of ver­te­brate skele­tal mus­cle (Fig­ure 2B). Pos­si­bly made from up to twelve dif­fer­ent gly­co­sy­lated fla­gellin pro­teins en­coded by MO‑1 (the high­est known num­ber of dif­fer­ent fla­gellins in a sin­gle bac­terium), the fla­gella and fib­rils are bun­dled to­gether within a sheath. This arrange­ment cre­ates a nearly ten-fold in­crease in the force of the fla­gel­lar beat as a bun­dle, com­pared to sin­gle, sep­a­rated fla­gella.

Fig­ure 3: (A) Swim­ming tra­jec­to­ries of E. coli and MO-. Note the dif­fer­ent time frames and scale bars. (B) Slice from a cryo-elec­tron mi­cro­graph show­ing fla­gella, F, and the mag­ne­to­some, M, il­lus­trated in top right cor­ner, high­light­ing that the mag­ne­to­some ap­pears of­ten per­pen­dic­u­lar to the axis of move­ment. Scale bar = 1 um. © Swim­ming be­hav­ior of MO‑1 cells in phase mi­croscopy when en­coun­ter­ing an agarose ob­sta­cle (cloudy re­gion) in the pres­ence of a mag­netic field. The paths of mul­ti­ple cells are tracked in unique col­ors over a pe­riod of 5.66 sec­onds. Bac­te­ria are swim­ming north­ward (from right to left). Adapted from: source

The Ben­e­fits of a Mag­netic Per­son­al­ity

So, why does MO‑1 make this spe­cially evolved fla­gel­lar struc­ture for its mag­ne­to­taxis? Where is it rac­ing to at such speeds, and just how im­por­tant is the mag­ne­to­some in this re­gard? As the quote above sug­gests, MO‑1 and re­lated bac­te­ria re­side in the first top cen­time­ters of ma­rine sed­i­ment, within the oxic/anoxic in­ter­face (OAI) where oxy­gen is present at low con­cen­tra­tions. The work­ing model is that mag­ne­to­somes al­low cells to align with the mag­netic field and swim into the OAI (ei­ther down from oxic en­vi­ron­ments through counter-clock­wise fla­gel­lar ro­ta­tion or up from anoxic en­vi­ron­ments through clock­wise fla­gel­lar ro­ta­tion). Once in the OAI sed­i­ment pock­ets, mag­ne­to­tac­tic bac­te­ria would still need to re­spond rapidly to the low nu­tri­ent con­di­tions, which are in con­stant flux.

In their re­cent re­port, the lab that iden­ti­fied and re­searched MO‑1 set out to fur­ther de­scribe its mag­ne­to­tac­tic be­hav­ior and char­ac­ter­ize its im­por­tance for the bac­te­ria. They found that in con­trast to the way E. coli swims (which is marked by short 'runs' in­ter­rupted ap­prox­i­mately once every half sec­ond by a di­rec­tion-chang­ing 'tum­ble'), MO‑1 swims more or less straight for rel­a­tively long time pe­ri­ods (up to 17 sec­onds) with no change in di­rec­tion (Fig­ure 3A). Sur­pris­ingly, the re­searchers found that un­like other in­ves­ti­gated cases, the mag­ne­to­some of MO‑1 does not ap­pear to align par­al­lel to the bacteria's di­rec­tion of move­ment, but rather are per­pen­dic­u­lar to it (Fig­ure 3B) The rea­son why the mag­ne­to­some of MO‑1 does not per­fectly align with mag­netic field lines, yet the bac­te­ria them­selves do, re­mains un­clear and high­lights how lit­tle we know re­gard­ing mag­ne­to­some struc­ture and func­tion.

To sim­u­late MO‑1 move­ment within its na­tive en­vi­ron­ment, the re­searchers ap­plied a uni­form mag­netic field to cul­tures that con­tained 'ob­sta­cles' con­sist­ing of large agarose ag­gre­gates as a proxy for the gran­u­lar na­ture of the sed­i­ment (Fig­ure 3C). While some MO‑1 cells squeezed through the agarose or be­came stuck, when many of the cells en­coun­tered the ob­sta­cle, they first turned away and then re­versed di­rec­tion against the mag­netic field (an­tipar­al­lel), and then turned to re­verse di­rec­tion again back onto their orig­i­nal course with only min­i­mal al­ter­ations from the orig­i­nal lin­ear path.

Fig­ure 4: MO‑1 in­oc­u­lated with in­di­cated cell num­bers into oxy­gen-per­me­able plas­tic tubes with growth me­dia. The tubes are then sealed and in­cu­bated for two days in the pres­ence (A) or ab­sence (B) of a ge­o­mag­netic field. The liq­uid menis­cus is in­di­cated (the dense white 'smile' at the top of each cul­ture) and growth as a glob­ule or dou­ble bands (up­per more in­tense due to more north-swim­ming bac­te­ria, pre­sum­ably) in the pres­ence of a mag­netic field (A), but only as a low den­sity swirl in the ab­sence of a mag­netic field (B). Adapted from: source

Fig­ure 4: MO‑1 in­oc­u­lated with in­di­cated cell num­bers into oxy­gen-per­me­able plas­tic tubes with growth me­dia. The tubes are then sealed and in­cu­bated for two days in the pres­ence (A) or ab­sence (B) of a ge­o­mag­netic field. The liq­uid menis­cus is in­di­cated (the dense white 'smile' at the top of each cul­ture) and growth as a glob­ule or dou­ble bands (up­per more in­tense due to more north-swim­ming bac­te­ria, pre­sum­ably) in the pres­ence of a mag­netic field (A), but only as a low den­sity swirl in the ab­sence of a mag­netic field (B). Adapted from: source

An es­pe­cially ex­cit­ing find­ing oc­curred when re­searchers com­pared MO‑1 growth in the pres­ence or ab­sence of a mag­netic field in a sharp gra­di­ent of oxy­gen con­cen­tra­tion (oxy­cline). With a ge­o­mag­netic field avail­able, MO‑1 cells in­oc­u­lated into oxy­gen-per­me­able plas­tic tubes ini­tially form a roundish glob­ule near the sur­face of the liq­uid and close to the side of the plas­tic tubes, fol­low­ing a grad­ual ver­ti­cal oxy­gen gra­di­ent from the liq­uid sur­face and a sharp ra­di­ate gra­di­ent from the oxy­gen-dif­fusible plas­tic tube walls. At low­est in­oc­u­la­tions, cells never reach a den­sity high enough to al­ter this zone of growth, even af­ter two days (Fig­ure 4A1).

With higher in­oc­u­la­tions, cell den­sity in­creases enough cells to form a thick, dense band around the di­am­e­ter (walls) of the tube. Even­tu­ally, af­ter two days, use of oxy­gen by the bac­te­ria for their res­pi­ra­tion (pre­sum­ably faster than the oxy­gen can dif­fuse in) leads to an al­tered re­dox po­ten­tial where that ini­tially formed band of dense growth has now formed a re­duced en­vi­ron­ment, prompt­ing the bac­te­ria to swim north­wards or south­wards to­wards the two OAIs (above and be­low) to cre­ate two new bands of growth (Fig­ure 4A2 – 4A4)

Re­mark­ably, the pres­ence of the mag­netic field is vi­tal for op­ti­mal MO‑1 growth in the pres­ence of these sharp oxy­gen (re­dox) gra­di­ents. Us­ing a spe­cially de­signed shield­ing de­vice that damp­ens the mag­netic field, the re­searchers found that even at rel­a­tively high in­ocu­lum den­si­ties MO‑1 cells were un­able to ad­just to chang­ing oxy­gen con­cen­tra­tions. Fig­ure 4B2 – 4B4). In the ab­sence of a mag­netic field MO‑1 cells formed, but per­sisted, as a round glob­ule af­ter two days, un­able to achieve high cell den­si­ties by swim­ming ef­fi­ciently into two new oxy­gen-rich en­vi­ron­ment bands. Strik­ingly, at the low­est cell den­sity in­ocu­lum (Fig­ure 4B1), the mag­netic field proved es­sen­tial for es­tab­lish­ing any growth at all (check­ing up to four days).

In­ter­est­ingly, MO‑1 cells still ap­pear to form mag­ne­to­somes in the ab­sence of the mag­netic field, they just don't use them to guide cell. To re­cap: in low-den­sity con­di­tions the mag­netic field went from be­ing op­ti­mal for MO‑1 growth to be­com­ing es­sen­tial. This sug­gests that mag­ne­to­taxis may in­deed have evolved to make use of the Earth's mag­netic field to re­spond rapidly for move­ment to mi­cro-zones with en­ergy avail­abil­ity. The au­thors also spec­u­late that, in ad­di­tion, the rapid swim­ming of MO‑1 may cause lo­cal con­vec­tive oxy­gen cur­rents that are more ef­fi­cient than sim­ple dif­fu­sion.

At­tract­ing More Ques­tions

When it comes to mag­ne­to­tac­tic bac­te­ria in gen­eral and to MO‑1 specif­i­cally, many ques­tions cer­tainly re­main. Not much is known about how the mag­ne­to­some (in the pres­ence of a mag­netic field) in­te­grates with the fla­gella, or how MO‑1 is able to sense an ob­sta­cle, briefly re­verse di­rec­tion, and then re­sume its near-orig­i­nal path. Ad­di­tion­ally it re­mains un­clear how in­di­vid­ual MO‑1 cells man­age to change swim­ming di­rec­tion be­yond the lin­ear paths ob­served in this pa­per. Study of strains like MO‑1 in spe­cially cre­ated mi­croflu­idic de­vices and cham­bers and the de­vel­op­ment of a ge­netic sys­tem could pull these in­ter­est­ing bac­te­ria to new poles of dis­cov­ery.

 

Daniel is a post­doc­toral fel­low in the Mar­golin Lab in the De­part­ment of Mi­cro­bi­ol­ogy & Mol­e­c­u­lar Ge­net­ics at the Uni­ver­sity of Texas, Hous­ton Med­ical School. He also teaches as an ad­junct pro­fes­sor at the Uni­ver­sity of Hous­ton-Down­town in the De­part­ment of Nat­ural Sci­ences. In ad­di­tion to sci­ence, he en­joys read­ing, writ­ing, and film. He can be found on Google+.