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Oceanic Fault Zones Reconstructed News & views energy regimes than those of aerobic eukar- mitochondria in eukaryotes. In both cases, res- production, has been replaced or retained in yotes. This kind of metabolism has arisen in piratory capacity was acquired by an anaerobic the ciliate’s hydrogenosomes. Evidence indicat- various types of anaerobic eukaryote, and is host cell through the metabolic integration of ing that the ATP transporter identified by Graf associated with the evolution of mitochon- a proteobacterial endosymbiont, and mecha- and colleagues can export ATP to the ciliate host dria into organelles called hydrogenosomes8. nisms can be identified for energy exchange would help to confirm the proposed symbiotic All hydrogenosomes have, to some degree, between symbiont and host cell. Furthermore, interaction. Further discovery and exploration lost mitochondrial pathways for aerobic res- a substantial reduction of the endosymbiont of similarly surprising symbiotic interactions in piration, and generate hydrogen rather than genome is observed, although mitochondrial poorly explored parts of the microbial world is carbon dioxide and water as an end product genomes are typically either much smaller than certainly an exciting prospect for the future. of their energy-generating pathways. Ciliates the endosymbiont genome observed by Graf are exceptionally effective at adapting to oxy- and colleagues, or have been lost completely William H. Lewis and Thijs J. G. Ettema are in gen-depleted environments, and mitochon- (as is the case for several hydrogenosomes10). the Laboratory of Microbiology, Wageningen drion-to-hydrogenosome transitions have Despite these fascinating similarities, there University and Research, NL-6708 WE occurred independently several times in this are also notable differences. Mitochondrial Wageningen, the Netherlands. W.H.L. is also in group of organisms9. endosymbiosis was a much more ancient the Department of Biochemistry, University of Graf and colleagues investigated an anaero- event, enlisting an archaeal host cell rather Cambridge, Cambridge, UK. bic ciliate belonging to the class Plagiopylea, than a modern eukaryotic cell. Mitochondria, e-mails: [email protected]; found in the deepest layers of Lake Zug in even if now reduced from their original form, [email protected] Switzerland. This environment lacks oxygen or even lost from some present-day eukar- 11 and contains relatively high levels of nitrate. yotes , became an integral part of eukary- 1. Graf, J. S. et al. Nature 591, 445–450 (2021). An initial assessment using microscopy otic cells. Genes inherited from the original 2. Eme, L., Spang, A., Lombard, J., Stairs, C. W. & revealed that, unusually, these ciliates have mitochondrial endosymbiont were often re­­ Ettema, T. J. G. Nature Rev. Microbiol. 15, 711–723 (2017). 3. Zaremba-Niedzwiedzka, K. et al. Nature 541, 353–358 a bacterial endosymbiont (belonging to the targeted to the nuclear genome, and some of (2017). class Gamma proteobacteria), rather than an the proteins these genes encoded adopted var- 4. Roger, A. J., Muñoz-Gómez, S. A. & Kamikawa, R. archaeal endosymbiont that produces meth- ious functions throughout the cell. A similar Curr. Biol. 27, R1177–R1192 (2017). 5. Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. Nature 506, ane, which is the more typical type of endo- level of integration is unlikely for the bacterial 307–315 (2014). symbiont present in anaerobic ciliates. endosymbionts of the ciliate investigated. 6. Betts, H. C. et al. Nature Ecol. Evol. 2, 1556–1562 (2018). DNA-sequencing data for lake-water sam- Nevertheless, it would be interesting to 7. Pittis, A. A. & Gabaldón, T. Nature 531, 101–104 (2016). 8. Embley, T. M. Phil. Trans. R. Soc. B 361, 1055–1067 (2006). ples revealed the presence of genes indicating study whether there has been any relocation 9. Embley, T. M. et al. Proc. R. Soc. Lond. B 262, 87–93 (1995). that the ciliate cells have hydrogenosomes. or repurposing of genes between the host 10. Lewis, W. H. et al. Mol. Biol. Evol. 37, 524–539 (2020). Moreover, the sequencing data indicate that and endosymbiont, and to what extent a 11. Karnkowska, A. et al. Curr. Biol. 26, 1274–1284 (2016). the bacterial endosymbionts have an elec- typical mitochondrial function, such as ATP This article was published online on 3 March 2021. tron-transport chain — a collection of protein complexes for respiration that enable energy Geophysics to be produced by a process called oxidative phosphorylation. Graf et al. propose that the electron acceptor in this chain is nitrate, rather than the oxygen used by aerobic organisms. Oceanic fault zones Consistent with this model, the authors report that rates of denitrification (the microbial pro- reconstructed cess that converts nitrate into nitrogen) were higher in lake-water samples in which ciliates Garrett Ito were present than in those from which ciliates had been removed. Tectonic-plate material is generally thought to be neither The genome of the endosymbiont identi- created nor destroyed at plate boundaries called oceanic fied by Graf and colleagues is notably smaller transform faults. An analysis of sea-floor topography suggests than the genomes of most endosymbionts of microbial eukaryotes, containing a mere that this assumption is incorrect. See p.402 310 protein-encoding genes. Among those, the authors identified a gene that encodes a poten- tial transporter protein for ATP, which they At undersea structures called oceanic spread- in a several-kilometre-wide region called the suggest is used to export ATP from the endo- ing centres, two tectonic plates split apart, and transform deformation zone, the crust gen- symbiont into its host, enabling the ciliate to molten rock from volcanic activity solidifies erated at one spreading segment undergoes use the endosymbiont for energy production to produce the crust of the sea floor. These episodes of thinning and then regrowth as it by ‘breathing’ nitrate. This finding represents spreading centres are separated into indi- drifts towards and past the adjacent segment. a unique example of an endosymbiont that has vidual segments that are tens to hundreds of Grevemeyer and colleagues’ work was ena- contributed the capacity for respiration (albeit kilometres long. At the ends of the segments, bled by international collaborations that have using nitrate instead of oxygen as an electron shearing (side-by-side sliding) of the two supported decades of seagoing expeditions acceptor) to a eukaryote that seemingly plates occurs along plate boundaries known to the world’s oceanic spreading centres. The retains organelles of mitochondrial descent as oceanic transform faults. Since their dis- authors analysed sea-floor topography around (hydrogenosomes) — the ancestral versions of covery in the mid-1960s1, these faults have the intersections between spreading-segment which once performed respiratory functions. been considered as sites where plate mater- ends and transform faults globally. At these Intriguingly, several parallels can be drawn ial is neither created nor destroyed. But on intersections, young crust produced at one between the cellular partnership discovered page 402, Grevemeyer et al.2 report that this spreading segment (the ‘proximal’ segment) is by Graf and co-workers and the evolution of description is too simplistic. They show that, adjacent to old crust that has been transported 376 | Nature | Vol 591 | 18 March 2021 ©2021 Spri nger Nature Li mited. All ri ghts reserved. ©2021 Spri nger Nature Li mited. All ri ghts reserved. have a widespread role in this new concept Proximal of transform-fault evolution. Moreover, the spreading segment authors make the striking observation that the amount of shoaling between the TDZ and the FZ seems to be independent of the spread- Oceanic Oceanic plate 1 Distal plate 2 ing rate. This finding suggests that the degree spreading Transform Young J-shaped of volcanic reconstruction is as high at cool, segment fault crust ridge magma-starved slow-spreading systems as it is at hot, magma-rich fast-spreading systems. Grevemeyer and colleagues’ discoveries Fracture zone and interpretations are compelling, but also demand further investigation. For example, Cracks and Old Volcanic valleys crust reconstruction future studies should aim to reconcile the Volcanic activity predicted horizontal stretching of the TDZ with the fact that earthquakes along oceanic transform faults are mainly associated with Crust 7 8 Plate motion shearing rather than stretching . More over, Rising Lithosphere further modelling work should examine magma whether the results of the authors’ model per- Asthenosphere sist under more-realistic conditions than those considered in their paper. For instance, such work could consider topography supported Figure 1 | Revised understanding of oceanic fault zones. Oceanic spreading centres are areas at which by dynamic stresses9, surface faults and state- two oceanic tectonic plates, consisting of a lithosphere (rigid layer) and crust, split apart. At spreading of-the-art deformation laws derived from rock centres, magma rises from a low-viscosity layer called the asthenosphere, and volcanic activity produces physics. the crust of the sea floor. Spreading centres are separated into segments connected by plate boundaries Regarding volcanic reconstruction, sea- known as oceanic transform faults. In a region called the transform deformation zone (TDZ; blue shaded floor seismic studies are needed to test the region), young crust created at the ‘proximal’ spreading
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