A Para­me­cium, a Pur­ple Bac­terium, and a Green Alga Walk into a Bar…

by Janie

"Three to tango" makes yet an­other ap­pear­ance in endo­symbioses, this time in the form of a pur­ple-green cil­iate that is home to both pur­ple bac­teria and green al­gae. At first glance, this seems like a para­dox. Pur­ple bac­teria are an­aerobic and an­oxygenic photo­synthesizers, but green al­gae are aer­obic and oxy­genic photo­synthesizers. To add to the baf­flement, the res­pective pur­ple and green photo­synthetic pig­ments ab­sorb at non-over­lap­ping wave­lengths. So how is it that this lit­tle cil­iated para­dox came to be?

Fig­ure 1. (A) A P. tenue cell, which con­tains nu­mer­ous pur­ple sul­fur bac­te­ria and green al­gae. Also vis­i­ble are a peri­s­tome ℗, a macronu­cleus (MA), and a pos­te­rior con­trac­tile vac­uole (CV). (B) P. tenue cy­to­plasm close-up with pur­ple bac­te­ria (B), green al­gae (A), and food vacu­oles (FV) with par­tially di­gested ma­te­r­ial. © Div­id­ing endo­symbiotic bac­teria are in­dicated by ar­rowheads. (D) Ellip­tical endo­sym­biotic al­gal cells are likely from auto­spore for­mation. Source. Fron­tis­piece is (B).

Pseudoble­phar­isma tenue is a para­mecium that was first des­cribed in 1926 by Al­fred Kahl. It then sat in ob­scurity for nearly a cen­tury un­til Muños-Gómez et al. re­covered the cil­iate from its home in the Sim­melried sphag­num ponds in Ger­many, where it co­exists with pur­ple bac­teria within hyp­oxic sed­iments. Micro­scopy rev­ealed that P. tenue is it­self home to num­erous pur­ple bac­terial cells and green al­gal cells, some of which could be im­aged in the mid­dle of div­ision (Fig­ure 1). The pur­ple bac­teria make up the maj­ority of the intra­cellular dwel­lers; each host con­tains 900 to 1300 of them.

P. tenue is a cur­ious hodge­podge of metab­olism. The green al­gae have chloro­plasts with py­renoid-like struc­tures, mito­chondria, and cyto­solic fer­ment­ative path­ways. The pur­ple bac­teria have lost some metab­olic path­ways found in other pur­ple sul­fur bac­teria (sul­fur dis­simil­ation and nit­rogen fixa­tion), but they can per­form aero­bic res­piration, an­oxygenic photo­synthesis, and fer­mentation. The host it­self has both mito­chondria and path­ways for fer­mentation, plus food vac­uoles that sug­gest that it also phago­cytoses food. So many modes of en­ergy prod­uction! Whether aer­obic or an­aerobic, light or dark, auto­trophic or hetero­trophic, P. tenue seems to have some­thing for every­thing.

Fig­ure 2. The ma­jor phys­i­o­log­i­cal modes of the P. tenue sym­bi­otic trio across two en­vi­ron­men­tal vari­ables, light in­ten­sity and oxy­gen con­cen­tra­tion. The dark ahadow­ing in­di­cates the niche of the sym­biotic trio. Source

Muños‑Gómez et al. sug­gest that des­pite all this ap­parent metab­olic flexi­bility, P. tenue is quite picky. The cil­i­ate is more of a Jekyll-and-Hyde mixo­troph. The au­thors sug­gest that dur­ing the day­time, it is in an­oxygenic mode, in which its mito­chondria and green al­gae fer­ment and pro­duce hy­drogen and small or­ganic mol­ecules that the pur­ple bac­teria then use for photo­synthesis. Dur­ing the night­time, all three part­ners turn to aer­obic res­piration, us­ing the food that's been stock­piled dur­ing the day through photo­synthesis and phago­cytosis. All in all, here is an un­usual micro­bial part­nership that recon­ciles div­erse modes of liv­ing.

A lin­gering ques­tion – how old and how sta­ble is this tri­partite endo­symbiosis? Deep-sea Rif­tia tube­worms de­grade and di­gest their endo­symbionts as a ma­jor source of en­ergy; could a sim­ilar turn­over be hap­pen­ing in P. tenue, the host per­haps pick­ing up re­placement res­idents through phago­cytosis?