A unique symbiosome in an anaerobic single-celled eukaryote

Abstract

Symbiotic relationships drive evolutionary change and are important sources of novelty. Here we demonstrate a highly structured syntrophic symbiosis between species of the anaerobic protistAnaeramoeba(Anaeramoebae, Metamonada) and bacterial ectosymbionts. We dissected this symbiosis with long-read metagenomics, transcriptomics of host and symbiont cells coupled with fluorescent in situ hybridization (FISH), and microscopy. Genome sequencing, phylogenomic analyses and FISH show that the symbionts belong to theDesulfobacteraceaeand were acquired independently in two differentAnaeramoebaspecies. We show that ectosymbionts likely reside deep within cell surface invaginations in a symbiosomal membrane network that is tightly associated with cytoplasmic hydrogenosomes. Metabolic reconstructions based on the genomes and transcriptomes of the symbionts suggest a highly evolved syntrophic interaction. Host hydrogenosomes likely produce hydrogen, acetate, and propionate that are consumed by the symbionts dissimilatory sulfate reduction, Wood-Ljungdahl and methylmalonyl pathways, respectively. Because the host genome sequences encode several vitamin B12-dependent enzymes but appear to lack the ability to biosynthesize this vitamin, we hypothesize that the symbionts supply their hosts with B12. We detected numerous lateral gene transfers from diverse bacteria toAnaeramoeba, including genes involved in oxygen defense and anaerobic metabolism. Gene families encoding membrane-trafficking components that regulate the phagosomal maturation machinery are notably expanded inAnaeramoebaspp. and may be involved in organizing and/or stabilizing the symbiosomal membrane system. Overall, the Anaeramoebae have evolved a dynamic symbiosome comprised of a vacuolar system that facilitates positioning and maintenance of sulfate-reducing bacterial ectosymbionts.

Anaeramoeba pumila sp. nov. and Anaeramoeba sp. OCE22C represent two novel types of symbiosis of Anaeramoebae and prokaryotes

“…13A in Táborský et al, 2017). Notably, Jerlström-Hultqvist et al (2023) showed that the membrane of symbiont vesicles is not continuous, that is, the "pouches" are actually deep invaginations of the cell membrane and their interior is in contact with the outer environment, at least in A. flamelloides and A. ignava. They also identified the symbionts as sulfate-reducing Deltaproteobacteria, which explains the importance of the access of the symbionts to the outer environment and relatively high sulfate concentrations of marine water.…”

“…The MROs form a cluster with symbiotic prokaryotes in the cytoplasm. It was shown only recently that the symbionts are sulfate-reducing Desulfobacter-related bacteria, which were acquired at least twice independently within the Anaeramoeba lineage (Jerlström-Hultqvist et al, 2023). Although they were originally considered endosymbionts by Táborský et al (2017), they likely reside within deep cell membrane invaginations and are exposed to the outer environment (Jerlström-Hultqvist et al, 2023).…”

“…It was shown only recently that the symbionts are sulfate-reducing Desulfobacter-related bacteria, which were acquired at least twice independently within the Anaeramoeba lineage (Jerlström-Hultqvist et al, 2023). Although they were originally considered endosymbionts by Táborský et al (2017), they likely reside within deep cell membrane invaginations and are exposed to the outer environment (Jerlström-Hultqvist et al, 2023). Host MROs produce propionate, acetate, and molecular hydrogen (Stairs et al, 2021), which are probably the key metabolites supporting the syntrophic interaction between Anaeramoeba and its symbionts.…”

“…Although they were originally considered endosymbionts by Táborský et al. (2017), they likely reside within deep cell membrane invaginations and are exposed to the outer environment (Jerlström‐Hultqvist et al., 2023). Host MROs produce propionate, acetate, and molecular hydrogen (Stairs et al., 2021), which are probably the key metabolites supporting the syntrophic interaction between Anaeramoeba and its symbionts.…”

“…Host MROs produce propionate, acetate, and molecular hydrogen (Stairs et al., 2021), which are probably the key metabolites supporting the syntrophic interaction between Anaeramoeba and its symbionts. In addition, the symbionts possibly supply their hosts with vitamin B12 (Jerlström‐Hultqvist et al., 2023).…”