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'Roots' in Mixotrophic Algae

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'Roots' in Mixotrophic Algae SCIENTIFIC CORRESPONDENCE B). The 16S ribosomal RNA sequences of 'Roots' in mixotrophic algae these organisms5 place bacterium A, a halophile, close to unnamed species of SIR - Macroalgae are thought to depend attached stolon and fronds in unlabelled Rhodopseudomonas in the Agrobacter­ on absorption of nutrients from the water sea water demonstrates significant uptake ium-Rhizobium group of branch-a proteo­ column because, unlike vascular plants, and translocation of 14C from rhizoids to bacteria, and bacterium B in the fluor­ they lack root systems with which to stolon and fronds (bin the figure). Previous escent Pseudomonas group of branch--y exploit nutrient resources in substrata 1• work has shown that NH! can be absorbed proteobacteria6• Bacterium A carries the Here we show that the giant marine by the rhizoids of C. cupressoides2• Uptake nifH gene, which encodes nitrogenase pro­ coenocyte, Caulerpa taxifolia, possesses a of nutrients from substrata explains why: duction 7. A Rhodopseudomonas-like bac­ 'root system' containing endocellular bac­ neither tissue nutrient content nor photo­ terium with the potential to fix N2 in the teria which can take up inorganic phos­ synthetic rate is correlated with seawater rhizoids of an alga has not been reported. phorus and organic nitrogen from nutrient concentration3; seasonal changes Caule,pa taxifolia has recently proliferat­ substrata and translocate nutrient prod­ in alkaline phosphatase activity are ed in the northwest Mediterranean on sub­ ucts to the photoassimilatory organs. The correlated with productivity and not sea­ strata that are heavily enriched in organic uptake of carbon, nitrogen and phospho­ water [PoJ-] (ref. 3), and elevation of matter, largely anoxic, perfused with hydro­ rus from substrata can explain the alga's seawater [POJ-] does not inhibit alkaline gen sulphide and contaminated with precip­ ability to proliferate in oligotrophic water. phosphatase activity, as occurs in other itated inorganic phosphorus. Oxygen Caulerpa taxifolia produces stolons, marine algae4• These data indicate that deficits in rhizoids rooted in anoxic sub­ fronds and gravipositive rhizoids which nutrient uptake from the water column is strata could support N2 fixation8•9, thus mimic the organs of a vascular plant. The subordinate to uptake from substrata. accelerating decomposition of high C:N rhizoids penetrate substrata and attach to Mixed bacteria coat the outer surfaces macrophyte vegetation8 and hence nutrient mineral surfaces. Chemical action at sites of of the rhizoids, whereas large numbers of supply to the alga. Removal of sulphide by a attachment releases mineral-bound nutri­ bacterial rods (104-105 mm-3) exist in the Rhodopseudomonas-like bacterium10 could ents such as inorganic phosphorus directly cytoplasm. We isolated several different give the alga a further advantage by protect­ to the alga (a in the figure). The rhizoids bacteria from cytoplasmic fluids aspirated ing its rhizoids. Catabolism of organic sub­ can also take up dissolved amino acid. from the rhizoids and cultured two Gram­ strates by endocellular and surface-borne Twin-compartment incubation of rhizoids negative, polarly flagellated, aerobic bac­ heterotrophs could supply CO2 for photo­ in 14C-valine-labelled sea water and teria, with differing urease activity (A and synthesis and partially explain the highly negative 013C tissue values ( <- 30%0) reported in other Caulerpa spp.11. Further research must establish how the alga and bacteria interact, whether N2 fix­ ation occurs, and the chemical mechanism by which inorganic phosphorus is acquired by the rhizoids. Our results show that the rhizoids of C. taxifolia function as 'roots' and can derive organic carbon and nitro­ gen, and inorganic phosphorus, directly from substrata. Rhizoid uptake of nutrients provides a physiological explanation for the success of siphonaceous green algae in oligotrophic tropical waters and the recent prolific development of C. taxifolia on eutrophic substrata in the northwest Mediterranean. J. R. M. Chisholm·, C. Dauga t E. Ageront, P.A. D. Grimontt J.M. Jaubert· * Unite des Enterobacteries, Unite 386 INSERM, lnstitut Pasteur, 75724 Paris Cedex 15, France tObservatoire 0ceano/ogique Europeen, Autoradiographs demonstrating uptake of inorganic and organic nutrients by the rhizoids of C. Centre Scientifique de Monaco, taxifolia and their subsequent translocation to the photoassimilatory stolons and fronds. a, We grew test and control samples of C. taxifolia adjacent to one another for 7 days in flow-throw MC 98000 Principality of Monaco aquaria containing a 1-cm-deep, aerated bed of coarse CaC03 sand (particle size 3- 5 mm) 33 3 1. Hanisak, M. D. in Nitrogen in the Marine Environment labelled with a surface precipitate of P-apatite (8.9 kBq cm- substrate). We prepared the pre­ (eds Carpenter, E. J. & Capone, D. G.) 699--730 cipitate by agitating the sand grains for 6 h in a minimal volume of sea water containing (Academic, New York, 1983). 33 33 H3 POt ; we removed non-precipitated P by flushing (6 h). We grew rhizoids of the test sam­ 2. Williams, S. L. Limnof. Oceanogr. 29, 374 - 379 (1984). ples for a 7-day period until they had penetrated and attached to the substratum; we prevented 3. Delgado, 0 . et al. Bot. Mar. 39, 61- 67 (1996). 4 . Delgado, 0 . & Lapointe, B. E. Coral Reefs 13, 151-161 rhizoids of control samples from making contact with the substratum. We then removed sam­ (1994). ples, rinsed them in fresh sea water, freed them of adhering sand grains, and pressed, dried 5. Dauga, C. et al. Res. Microbial. 144, 35-46 (1993). and autoradiographed them. Test samples showed strong uptake of 33P by the rhizoids and 6 . Maidak, B. L. et al. Nucleic Acids Res. 22, 3485-3487 translocation of 33P to the photoassimilatory parts, whereas control samples failed to produce (1994). 7. Zehr, J. P. & Reynolds, L. A. Appl. envir. Microbial. 55, b, an image on the autoradiographic fi lm plate. We incubated rhizoids in sea water containing 2522- 2526 (1989). 14C-valine (11.1 kBq mI-1 ) in one half of a slotted, twin-compartment , incubation vessel that 8 . Paerl, H. W. in Advances in Microbial Ecology Vol. II (ed. allowed adjoining stolon and fronds to be incubated simultaneously in unlabelled sea water. Marshall, K. C.) 305- 337 (Plenum, New York, 1990). Communication between the two incubation compartments (other than through the algal siphon) 9. Villbrandt. M., Krumbein, W. E. & Stal, L. J. Kiefer Meeresforsch .. Sonderh. 8, 158-163 (1991). was prevented by sealing the junction between them with Vaseline, and gaseous exchange of 10. Hansen, T. A. & van Gemerden, H. Arch. Mikrobio/. 86, 14 14 respired C02 was prevented by capping the rhizoid compartment. Significant uptake of C­ 49- 56 (1972). valine by the rhizoids, and translocation of 14C to the stolon and fronds, occurred after 20 h. 11. Raven, J. A. et al. Mar. Ecol. Prag. Ser. 123, 193- 205 (1995). 382 NATURE · VOL 381 · 30 MAY 1996 .
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