Diversity and Evolutionary History of the Symbiontida (Euglenozoa)

Abstract

Several lineages of euglenozoans are enveloped with epibiotic bacteria and live in low oxygen and anoxic marine sediments, such as Bihospites bacati and Calkinsia aureus. A combination of shared ultrastructural traits and molecular phylogenetic inferences demonstrate that these lineages belong to a clade called the "Symbiontida." Bihospites and Calkinsia possess all of the synapomorphies for the Euglenozoa plus several novel traits. Bihospites has a distinctive cell surface organization reminiscent of the pellicle strips in euglenids, a robust C-shaped feeding apparatus that encircles the nucleus, and a diverse community of epibiotic bacteria. Calkinsia has a novel "extrusomal pocket" and a thick (orange) extracellular matrix beneath a uniform layer of epibiotic bacteria. Despite the absence of molecular phylogenetic data, similar ultrastructural traits in Postgaardi mariagerensis and its epibiotic bacteria strongly suggest that this species is also a member of the Symbiontida. Molecular phylogenetic trees inferred from small subunit (SSU) ribosomal DNA sequences have shown that Bihospites and Calkinsia group strongly with a diverse set of environmental DNA sequences (eDNA) generated from low-oxygen marine samples collected at different depths from different locations around the world. These data demonstrate a diverse array of symbiontids that have yet to be characterized at the genomic, cellular, and behavior levels, which underscores how poorly we currently understand the biology and ecology of the group. Moreover, current data suggest that the communities of epibiotic bacteria associated with Bihospites, Calkinsia, and Postgaardi co-evolved with their hosts and are metabolically integrated with modified mitochondria positioned immediately beneath the host's plasma membrane. No symbiontid species has ever been cultivated, so improved knowledge about these eukaryotic organisms and their intimate relationships with bacteria in low oxygen environments will likely be achieved using culture-independent approaches, such as isolated-cell metagenomics.

Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist

“…Magnetic protists from the Southern Hemisphere also had a swimming direction opposite to that expected for magnetotactic organisms 16 . All protists shared the same phenotypic traits, exhibiting synapomorphies defined for the Euglenozoa; for example, all have two flagella with reinforced heteromorphic paraxonemal rods 5 (that is, one dorsal flagellum with a tubular rod and one ventral flagellum with a lattice structure; Fig. 2c).…”

“…Widely distributed in the microbial world, particularly in anoxic settings 2,3 , they often rely on metabolic exchanges and syntrophy 2,4 . 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 syntrophy 6 .…”

“…The acquisition of organics might occur via diffusion out of the bacteria coupled to protist osmotrophy, although direct evidence for this is lacking. However, it might also happen by direct predation as in other Euglenozoa 5 . Several observations indicate that these magnetotactic protists are bacteriovorous phagotrophs capable, among others, of consuming their ectosymbiotic bacteria: (1) the presence of a rod-based feeding apparatus and a tubular cytostome, (2) the predation behaviour observed under the light microscope and (3) the presence of cells with partially dissolved magnetosomes in digestive vacuoles as has already been observed in other grazers 32 (Fig.…”

Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses

“…Symbiontids are marine heterotrophs, presumably phagotrophs, as suggested by their ultrastructure. Additionally, the bacteria on their surface probably exchange metabolites with the hosts' mitochondria-related organelles, and it is also possible that they provide a food source for the symbiontids [ 7 ].…”

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].…”