Genome analysis of ‘<i>Candidatus</i> Ancillula trichonymphae’, first representative of a deep‐branching clade of <i>Bifidobacteriales</i>, strengthens evidence for convergent evolution in flagellate endosymbionts

Strassert, Jürgen F. H.; Mikaelyan, Aram; Woyke, Tanja; Brune, Andreas

doi:10.1111/1758-2229.12451

Cited by 19 publications

(20 citation statements)

References 31 publications

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“…An interesting case of evolutionary convergence has been observed in "Candidatus Ancillula trichonymphae," an obligately intracellular actinobacterium that not only colonizes the same type of microhabitat as "Ca. Endomicrobium trichonymphae" but may also occupy a similar ecological niche (38,39). Also, this endosymbiont has experienced a substantial genome reduction and lacks dedicated transport systems for glucose and hexokinase (39).…”

Section: Discussionmentioning

confidence: 99%

“…Endomicrobium trichonymphae" but may also occupy a similar ecological niche (38,39). Also, this endosymbiont has experienced a substantial genome reduction and lacks dedicated transport systems for glucose and hexokinase (39). However, it retained a transporter for glycerol 3-phosphate (GlpT), which belongs to the same family of MFS transporters as UhpC (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Outlook. There is a growing body of evidence for convergent evolution among unrelated endosymbionts of termite gut flagellates (39)(40)(41). Endomicrobia provide an excellent model for future studies on the evolutionary mechanisms of symbiogenesis.…”

Section: Discussionmentioning

confidence: 99%

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Genome Analysis of Endomicrobium proavitum Suggests Loss and Gain of Relevant Functions during the Evolution of Intracellular Symbionts

Zheng

Dietrich

Brune

2017

Appl Environ Microbiol

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Bacterial endosymbionts of eukaryotes show progressive genome erosion, but detailed investigations of the evolutionary processes involved in the transition to an intracellular lifestyle are generally hampered by the lack of extant free-living lineages. Here, we characterize the genome of the recently isolated, free-living , the second member of the phylum brought into pure culture, and compare it to the closely related " Endomicrobium trichonymphae" strain Rs-D17, a previously described but uncultured endosymbiont of termite gut flagellates. A reconstruction of the metabolic pathways of matched the fermentation products formed in pure culture and underscored its restriction to glucose as the substrate. However, several pathways present in the free-living strain, e.g., for the uptake and activation of glucose and its subsequent fermentation, ammonium assimilation, and outer membrane biogenesis, were absent or disrupted in the endosymbiont, probably lost during the massive genome rearrangements that occurred during symbiogenesis. While the majority of the genes in strain Rs-D17 have orthologs in, the endosymbiont also possesses a number of functions that are absent from the free-living strain and may represent adaptations to the intracellular lifestyle. Phylogenetic analysis revealed that the genes encoding glucose 6-phosphate and amino acid transporters, acetaldehyde/alcohol dehydrogenase, and the pathways of glucuronic acid catabolism and thiamine pyrophosphate biosynthesis were either acquired by horizontal gene transfer or may represent ancestral traits that were lost in the free-living strain. The polyphyletic origin of in different flagellate hosts makes them excellent models for future studies of convergent and parallel evolution during symbiogenesis. The isolation of a free-living relative of intracellular symbionts provides the rare opportunity to identify the evolutionary processes that occur in the course of symbiogenesis. Our study documents that the genome of " Endomicrobium trichonymphae," which represents a clade of endosymbionts that have coevolved with termite gut flagellates for more than 40 million years, is not simply a subset of the genes present in , a member of the ancestral, free-living lineage. Rather, comparative genomics revealed that the endosymbionts possess several relevant functions that were either prerequisites for colonization of the intracellular habitat or might have served to compensate for genes losses that occurred during genome erosion. Some gene sets found only in the endosymbiont were apparently acquired by horizontal transfer from other gut bacteria, which suggests that the intracellular bacteria of flagellates are not entirely cut off from gene flow.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Genome Analysis of Endomicrobium proavitum Suggests Loss and Gain of Relevant Functions during the Evolution of Intracellular Symbionts

Zheng

Dietrich

Brune

2017

Appl Environ Microbiol

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“…This complex animal-protist-bacteriaarchaea community is a classic example of symbioses, but we lack much detail on the functional interactions between the partners, even after over a century of study. Genomic analyses are beginning to reveal the roles of symbiotic bacteria, which have retained metabolic pathways involved in the synthesis of vitamins, amino acids, and nucleotides, as well as the ability to fix nitrogen (4,5), suggesting that they provide critical nutrients to the protist and animal hosts. However, much of this information comes from a taxonomically narrow group of hosts, mainly species of Trichonympha (4-7), Pseudotrichonympha (8), Barbulanympha (9), and Eucomonympha (10), all members of the same parabasalian class.…”

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Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Treitli

Kolísko

Husník

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Lower termites harbor in their hindgut complex microbial communities that are involved in the digestion of cellulose. Among these are protists, which are usually associated with specific bacterial symbionts found on their surface or inside their cells. While these form the foundations of a classic system in symbiosis research, we still know little about the functional basis for most of these relationships. Here, we describe the complex functional relationship between one protist, the oxymonad Streblomastix strix, and its ectosymbiotic bacterial community using single-cell genomics. We generated partial assemblies of the host S. strix genome and Candidatus Ordinivivax streblomastigis, as well as a complex metagenome assembly of at least 8 other Bacteroidetes bacteria confirmed by ribosomal (r)RNA fluorescence in situ hybridization (FISH) to be associated with S. strix. Our data suggest that S. strix is probably not involved in the cellulose digestion, but the bacterial community on its surface secretes a complex array of glycosyl hydrolases, providing them with the ability to degrade cellulose to monomers and fueling the metabolism of S. strix. In addition, some of the bacteria can fix nitrogen and can theoretically provide S. strix with essential amino acids and cofactors, which the protist cannot synthesize. On the contrary, most of the bacterial symbionts lack the essential glycolytic enzyme enolase, which may be overcome by the exchange of intermediates with S. strix. This study demonstrates the value of the combined single-cell (meta)genomic and FISH approach for studies of complicated symbiotic systems.

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“…In addition, the nuclei of some hindgut protist species are colonized by Verrucomicrobia (12). Genome analysis of some of these endosymbionts, and some ectosymbionts, suggests that there is convergent evolution for these symbionts to support their unicellular host by synthesizing nutrients absent in the termites' diet (11,13,14). Regarding Endomicrobium, previous studies have investigated both their population structure and transmission in Trichonympha spp.…”

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Single-Cell Amplicon Sequencing Reveals Community Structures and Transmission Trends of Protist-Associated Bacteria in a Termite Host

Stephens

Gage

2018

Preprint

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The hindgut protists of wood-feeding termites are usually colonized by prokaryotic symbionts. Many of the hurdles that have prevented a better understanding of these symbionts arise from variation among protist and termite host species and the inability to maintain prominent community members in culture. These issues have made it difficult to study the fidelity, acquisition, and differences in colonization of protists by bacterial symbionts. In this study, we use high throughput amplicon sequencing of the V4 region of 16S rRNA genes to determine the composition of bacterial communities associated with single protist cells of six protist species, from the genera Pyrsonympha, Dinenympha, and Trichonympha that are present in the hindgut of the termite Reticulitermes flavipes. By analyzing amplicon sequence variants (ASVs), the diversity and distribution of protist-associated bacteria was compared within and across these six different protist species. ASV analysis showed that, in general, each protist genus associated with a distinct community of bacterial symbionts which were conserved across different termite colonies. However, some ASVs corresponding to ectosymbionts (Spirochaetes) were shared between different Dinenympha species and to a lesser extent with Pyrsonympha and Trichonympha hosts. This suggested that certain bacterial symbionts may be cosmopolitan to some degree and perhaps acquired by horizontal transmission. Using a fluorescence-based cell assay, we could observe the horizontal acquisition of surface-bound bacteria.This acquisition was shown to be time-dependent, involve active processes, and was non-random with respect to binding locations on some protists. Introduction ASV Inference of Protist-Associated Bacteria 2The lower termite R. flavipes harbors symbionts from the three domains of life, all of which make significant contributions to the digestion of lignocellulose and provisioning of essential nutrients. These symbionts include uncultivated hindgut protists of two eukaryotic taxa, Oxymonadida (order) and Parabasalia (phylum or class) (1,2). Most, and perhaps all, of these protists are colonized by both endo-and ectosymbionts belonging to various bacterial taxa (2).These protist-associated bacteria often exhibit complex community structures and occupy different sites on and within their unicellular hosts (2).Previous studies have shown that Oxymonadida protists in Reticulitermes speratus are co-colonized with Treponema ectosymbionts from two distinct phylogenetic clusters (Termite Treponema clusters I and II) (3,4) as well as a member of the Bacteroidales (5). These three ectosymbiotic lineages attach by one cell pole to the plasma membrane of their host (6) and exhibit intermixed colonization (5). Other known ectosymbionts include a Desulfovibrio species which embeds in the membrane of its host, Trichonympha (7). Functional and genomic data regarding the nature of these symbioses are limited but growing (8,9).The endosymbionts which colonize the cytoplasm of hindgut protists of Reticulitermes...

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Genome analysis of ‘Candidatus Ancillula trichonymphae’, first representative of a deep‐branching clade of Bifidobacteriales, strengthens evidence for convergent evolution in flagellate endosymbionts

Cited by 19 publications

References 31 publications

Genome Analysis of Endomicrobium proavitum Suggests Loss and Gain of Relevant Functions during the Evolution of Intracellular Symbionts

Genome Analysis of Endomicrobium proavitum Suggests Loss and Gain of Relevant Functions during the Evolution of Intracellular Symbionts

Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Single-Cell Amplicon Sequencing Reveals Community Structures and Transmission Trends of Protist-Associated Bacteria in a Termite Host

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