Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist

Abstract

Mutualistic symbioses are often a source of evolutionary innovation and drivers of biological diversification1. Widely distributed in the microbial world, particularly in anoxic settings2,3, they often rely on metabolic exchanges and syntrophy2,4. Here, we report a mutualistic symbiosis observed in marine anoxic sediments between excavate protists (Symbiontida, Euglenozoa)5 and ectosymbiotic Deltaproteobacteria biomineralizing ferrimagnetic nanoparticles. Light and electron microscopy observations as well as genomic data support a multi-layered mutualism based on collective magnetotactic motility with division of labour and interspecies hydrogen-transfer-based syntrophy6. The guided motility of the consortia along the geomagnetic field is allowed by the magnetic moment of the non-motile ectosymbiotic bacteria combined with the protist motor activity, which is a unique example of eukaryotic magnetoreception7 acquired by symbiosis. The nearly complete deltaproteobacterial genome assembled from a single consortium contains a full magnetosome gene set8, but shows signs of reduction, with the probable loss of flagellar genes. Based on the metabolic gene content, the ectosymbiotic bacteria are anaerobic sulfate-reducing chemolithoautotrophs that likely reduce sulfate with hydrogen produced by hydrogenosome-like organelles6 underlying the plasma membrane of the protist. In addition to being necessary hydrogen sinks, ectosymbionts may provide organics to the protist by diffusion and predation, as shown by magnetosome-containing digestive vacuoles. Phylogenetic analyses of 16S and 18S ribosomal RNA genes from magnetotactic consortia in marine sediments across the Northern and Southern hemispheres indicate a host–ectosymbiont specificity and co-evolution. This suggests a historical acquisition of magnetoreception by a euglenozoan ancestor from Deltaproteobacteria followed by subsequent diversification. It also supports the cosmopolitan nature of this type of symbiosis in marine anoxic sediments.

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes

“…Studies of magnetotactic protists would likely provide significant additional information in the evolution of magnetoreception in organisms that respond in some way to the Earth's magnetic field. Recently, Monteil and colleagues () described a mechanism of magnetite‐based magnetoreception in a consortium of a non‐motile deltaproteobacterium capable of producing magnetite magnetosomes and a flagellated non‐magnetotactic protist. The authors suggest that these bacterial and eukaryotic species coevolved resulting in an ancient acquisition of magnetoreception by protist from a deltaproteobacterium that biomineralizes magnetosomes (Monteil et al ., ).…”

“…Recently, Monteil and colleagues () described a mechanism of magnetite‐based magnetoreception in a consortium of a non‐motile deltaproteobacterium capable of producing magnetite magnetosomes and a flagellated non‐magnetotactic protist. The authors suggest that these bacterial and eukaryotic species coevolved resulting in an ancient acquisition of magnetoreception by protist from a deltaproteobacterium that biomineralizes magnetosomes (Monteil et al ., ). Results from further studies involving the ultrastructure and genome sequences of protists displaying magnetotactic behaviour should be important in determining other significant symbiotic events in the evolution of magnetoreception, the development of eukaryotes and of life itself.…”

Magnetoreception in Microorganisms

“…The recent discovery of magnetotactic holobionts changed our vision of magnetoreception in unicellular eukaryotes. A magnetotactic protist belonging to the Euglenozoa, Excavates, was observed in marine sediments worldwide [12,62]. Its magnetoreception was the result of a cooperation with ectosymbiotic bacteria with whom they live in a mutualistic symbiosis ( Figure 3) [12].…”

“…A magnetotactic protist belonging to the Euglenozoa, Excavates, was observed in marine sediments worldwide [12,62]. Its magnetoreception was the result of a cooperation with ectosymbiotic bacteria with whom they live in a mutualistic symbiosis ( Figure 3) [12]. Again, magnetoreception is magnetite-based and originates from prokaryotes biomineralizing magnetosomes chains.…”

“…This behaviour, called magnetotaxis, was until recently, observed in magnetotactic bacteria only. However, recent discoveries revealed that some unicellular eukaryotes in different phylogenetic groups are magnetotactic or at least become transiently magnetoreceptive by different mechanisms and interactions [11,12]. Here, we propose to review the diversity and different strategies microbes have developed to obtain their magnetic sense.…”