Impacts of a novel defensive symbiosis on the nematode host microbiome

AbstractHeritable microorganisms play critical roles in life cycles of many macro-organisms but their prevalence and functional roles are unknown for most plants. Bioactive ergot alkaloids produced by heritable Periglandula fungi occur in some morning glories (Convolvulaceae), similar to ergot alkaloids in grasses infected with related fungi. Ergot alkaloids have been of longstanding interest given their toxic effects, psychoactive properties, and medical applications. Here we show that ergot alkaloids are concentrated in four morning glory clades exhibiting differences in alkaloid profiles and are more prevalent in species with larger seeds than those with smaller seeds. Further, we found a phylogenetically-independent, positive correlation between seed mass and alkaloid concentrations in symbiotic species. Our findings suggest that heritable symbiosis has diversified among particular clades by vertical transmission through seeds combined with host speciation, and that ergot alkaloids are particularly beneficial to species with larger seeds. Our results are consistent with the defensive symbiosis hypothesis where bioactive ergot alkaloids from Periglandula symbionts protect seeds and seedlings from natural enemies, and provide a framework for exploring microbial chemistry in other plant-microbe interactions.

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Metagenomic exploration of the marine sponge mycale hentscheli uncovers multiple polyketide-producing bacterial symbionts

10.26686/wgtn.12444086 ◽

2020 ◽

Author(s):

Mathew Storey ◽

SK Andreassend ◽

Joe Bracegirdle ◽

Alistair Brown ◽

Robert Keyzers ◽

...

Keyword(s):

Marine Sponge ◽

Bacterial Species ◽

Gene Clusters ◽

Taxonomic Diversity ◽

Marine Sponges ◽

Metagenomic Sequencing ◽

Defensive Symbiosis ◽

Long Read ◽

Comprehensive Picture ◽

Mycale Hentscheli

© 2020 Storey et al. Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metag-enomic investigation of Mycale hentscheli, a chemically gifted marine sponge that pos-sesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short-and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemo-types. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holo-biont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These re-sults suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small mol-ecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing mi-crobe. We also find that the microbiome of M. hentscheli is stably maintained among in-dividuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.

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Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1400457111 ◽

2014 ◽

Vol 111 (17) ◽

pp. 6359-6364 ◽

Cited By ~ 66

Author(s):

M. Kaltenpoth ◽

K. Roeser-Mueller ◽

S. Koehler ◽

A. Peterson ◽

T. Y. Nechitaylo ◽

...

Keyword(s):

Partner Choice ◽

Defensive Symbiosis

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Defensive symbiosis in the real world - advancing ecological studies of heritable, protective bacteria in aphids and beyond

Functional Ecology ◽

10.1111/1365-2435.12133 ◽

2013 ◽

Vol 28 (2) ◽

pp. 341-355 ◽

Cited By ~ 194

Author(s):

Kerry M. Oliver ◽

Andrew H. Smith ◽

Jacob A. Russell

Keyword(s):

Real World ◽

Ecological Studies ◽

The Real ◽

Defensive Symbiosis

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Biogeography of a defensive symbiosis

Communicative & Integrative Biology ◽

10.4161/19420889.2014.993265 ◽

2014 ◽

Vol 7 (6) ◽

pp. e993265 ◽

Cited By ~ 3

Author(s):

Martin Kaltenpoth ◽

Kerstin Roeser-Mueller ◽

J. William Stubblefield ◽

Jon Seger ◽

Erhard Strohm

Keyword(s):

Defensive Symbiosis

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Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila

PLoS Pathogens ◽

10.1371/journal.ppat.1006431 ◽

2017 ◽

Vol 13 (7) ◽

pp. e1006431 ◽

Cited By ~ 34

Author(s):

Matthew J. Ballinger ◽

Steve J. Perlman

Keyword(s):

Parasitic Wasps ◽

Ribosome Inactivating Proteins ◽

Defensive Symbiosis

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A ribosome-inactivating protein in a Drosophila defensive symbiont

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1518648113 ◽

2015 ◽

Vol 113 (2) ◽

pp. 350-355 ◽

Cited By ~ 53

Author(s):

Phineas T. Hamilton ◽

Fangni Peng ◽

Martin J. Boulanger ◽

Steve J. Perlman

Keyword(s):

Ribosomal Rna ◽

28S Rrna ◽

Ribosome Inactivating Protein ◽

Defensive Symbiosis ◽

Rapid Spread ◽

A Cell ◽

Underlying Mechanisms ◽

Dependent Modification ◽

Dependent Mechanism

Vertically transmitted symbionts that protect their hosts against parasites and pathogens are well known from insects, yet the underlying mechanisms of symbiont-mediated defense are largely unclear. A striking example of an ecologically important defensive symbiosis involves the woodland fly Drosophila neotestacea, which is protected by the bacterial endosymbiont Spiroplasma when parasitized by the nematode Howardula aoronymphium. The benefit of this defense strategy has led to the rapid spread of Spiroplasma throughout the range of D. neotestacea, although the molecular basis for this protection has been unresolved. Here, we show that Spiroplasma encodes a ribosome-inactivating protein (RIP) related to Shiga-like toxins from enterohemorrhagic Escherichia coli and that Howardula ribosomal RNA (rRNA) is depurinated during Spiroplasma-mediated protection of D. neotestacea. First, we show that recombinant Spiroplasma RIP catalyzes depurination of 28S rRNAs in a cell-free assay, as well as Howardula rRNA in vitro at the canonical RIP target site within the α-sarcin/ricin loop (SRL) of 28S rRNA. We then show that Howardula parasites in Spiroplasma-infected flies show a strong signal of rRNA depurination consistent with RIP-dependent modification and large decreases in the proportion of 28S rRNA intact at the α-sarcin/ricin loop. Notably, host 28S rRNA is largely unaffected, suggesting targeted specificity. Collectively, our study identifies a novel RIP in an insect defensive symbiont and suggests an underlying RIP-dependent mechanism in Spiroplasma-mediated defense.

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Metagenomic Exploration of the Marine Sponge Mycale hentscheli Uncovers Multiple Polyketide-Producing Bacterial Symbionts

mBio ◽

10.1128/mbio.02997-19 ◽

2020 ◽

Vol 11 (2) ◽

Cited By ~ 5

Author(s):

Mathew A. Storey ◽

Sarah K. Andreassend ◽

Joe Bracegirdle ◽

Alistair Brown ◽

Robert A. Keyzers ◽

...

Keyword(s):

Marine Sponge ◽

Bacterial Species ◽

Gene Clusters ◽

Taxonomic Diversity ◽

Marine Sponges ◽

Metagenomic Sequencing ◽

Content Type ◽

Defensive Symbiosis ◽

Long Read ◽

Mycale Hentscheli

ABSTRACT Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metagenomic investigation of Mycale hentscheli, a chemically gifted marine sponge that possesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short- and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemotypes. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holobiont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These results suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small molecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing microbe. We also find that the microbiome of M. hentscheli is stably maintained among individuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.

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Phage loss and the breakdown of a defensive symbiosis in aphids

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2012.2103 ◽

2013 ◽

Vol 280 (1751) ◽

pp. 20122103 ◽

Cited By ~ 56

Author(s):

S. R. Weldon ◽

M. R. Strand ◽

K. M. Oliver

Keyword(s):

Acyrthosiphon Pisum ◽

Bacterial Symbiont ◽

Parasitoid Wasps ◽

Bacterial Symbionts ◽

Delayed Onset ◽

Lower Weight ◽

Terrestrial Arthropods ◽

Defensive Symbiosis ◽

Hamiltonella Defensa ◽

Secondary Endosymbiont

Terrestrial arthropods are often infected with heritable bacterial symbionts, which may themselves be infected by bacteriophages. However, what role, if any, bacteriophages play in the regulation and maintenance of insect–bacteria symbioses is largely unknown. Infection of the aphid Acyrthosiphon pisum by the bacterial symbiont Hamiltonella defensa confers protection against parasitoid wasps, but only when H. defensa is itself infected by the phage A. pisum secondary endosymbiont (APSE). Here, we use a controlled genetic background and correlation-based assays to show that loss of APSE is associated with up to sevenfold increases in the intra-aphid abundance of H. defensa . APSE loss is also associated with severe deleterious effects on aphid fitness: aphids infected with H. defensa lacking APSE have a significantly delayed onset of reproduction, lower weight at adulthood and half as many total offspring as aphids infected with phage-harbouring H. defensa , indicating that phage loss can rapidly lead to the breakdown of the defensive symbiosis. Our results overall indicate that bacteriophages play critical roles in both aphid defence and the maintenance of heritable symbiosis.

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