Evolution of specialized toxin arsenals in a bacterial symbiont of arthropods

Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments. Many toxin-encoding bacteria have evolved into host-associated defensive partnerships, in which they use toxins to improve host survival during...

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Vydané v:	The ISME Journal Ročník 19; číslo 1
Hlavní autori:	Moore, Logan D, Ballinger, Matthew J
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	England Oxford University Press 01.01.2025
Predmet:	Adenine Animals Arthropods Arthropods - microbiology Bacteria Bacterial Toxins - genetics Bacterial Toxins - metabolism Biocompatibility Damage Deactivation E coli Escherichia coli - genetics Escherichia coli - metabolism Evolution Evolution, Molecular Insects Localization Parasites Proteins Ribonucleic acid Ribosome Inactivating Proteins - genetics Ribosome Inactivating Proteins - metabolism Ribosomes Ribosomes - drug effects Ribosomes - metabolism Ricin RNA Spiroplasma - genetics Spiroplasma - metabolism Spiroplasma - physiology Stability Survival Symbionts Symbiosis Toxicity Toxins parasitism Spiroplasma ribosome-inactivating proteins defense symbiosis toxins
ISSN:	1751-7362, 1751-7370, 1751-7370
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Abstract	Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments. Many toxin-encoding bacteria have evolved into host-associated defensive partnerships, in which they use toxins to improve host survival during infection. The stability of these relationships requires that symbiont toxins target diverse parasites while minimizing damage to the host. We investigate the specificity of a group of ribosome-targeting toxins (ribosome-inactivating proteins) encoded by heritable Spiroplasma symbionts that contribute to defense against parasite infection in fruit fly hosts. Using Escherichia coli to express five divergent copies of this toxin, we show that distantly related members of the family all retain the ability to inactivate ribosomes by adenine cleavage at the α-sarcin/ricin loop, the enzymatic hallmark of RIPs. However, when exposed to live insect and fungal cells, ribosome inactivation varies across the five toxins, suggesting cellular recognition or localization play a role in target specificity. To identify toxin domains required for specificity, we removed rapidly evolving “accessory” domains from two toxins. Both truncated toxins exhibit significantly increased activity on purified ribosomes in vitro, suggesting one role of accessory domains is to reduce toxicity, which may help protect hosts from collateral damage. One of the truncated toxins also showed significantly reduced inactivation of cellular ribosomes in vivo, indicating a role for accessory domains in cell specificity. Together, these data reveal a mechanism for symbiont discrimination between hosts and parasites and highlight how dynamic toxin evolution can contribute to stability and novelty in defensive symbiosis.
AbstractList	Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments. Many toxin-encoding bacteria have evolved into host-associated defensive partnerships, in which they use toxins to improve host survival during infection. The stability of these relationships requires that symbiont toxins target diverse parasites while minimizing damage to the host. We investigate the specificity of a group of ribosome-targeting toxins (ribosome-inactivating proteins) encoded by heritable Spiroplasma symbionts that contribute to defense against parasite infection in fruit fly hosts. Using Escherichia coli to express five divergent copies of this toxin, we show that distantly related members of the family all retain the ability to inactivate ribosomes by adenine cleavage at the α-sarcin/ricin loop, the enzymatic hallmark of RIPs. However, when exposed to live insect and fungal cells, ribosome inactivation varies across the five toxins, suggesting cellular recognition or localization play a role in target specificity. To identify toxin domains required for specificity, we removed rapidly evolving “accessory” domains from two toxins. Both truncated toxins exhibit significantly increased activity on purified ribosomes in vitro, suggesting one role of accessory domains is to reduce toxicity, which may help protect hosts from collateral damage. One of the truncated toxins also showed significantly reduced inactivation of cellular ribosomes in vivo, indicating a role for accessory domains in cell specificity. Together, these data reveal a mechanism for symbiont discrimination between hosts and parasites and highlight how dynamic toxin evolution can contribute to stability and novelty in defensive symbiosis. Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments. Many toxin-encoding bacteria have evolved into host-associated defensive partnerships, in which they use toxins to improve host survival during infection. The stability of these relationships requires that symbiont toxins target diverse parasites while minimizing damage to the host. We investigate the specificity of a group of ribosome-targeting toxins (RIPs) encoded by heritable Spiroplasma symbionts that contribute to defense against parasite infection in fruit fly hosts. Using E. coli to express five divergent copies of this toxin, we show that distantly related members of the family all retain the ability to inactivate ribosomes by adenine cleavage at the α-sarcin/ricin loop, the enzymatic hallmark of RIPs. However, when exposed to live insect and fungal cells, ribosome inactivation varies across the five toxins, suggesting cellular recognition or localization play a role in target specificity. To identify toxin domains required for specificity, we removed rapidly evolving "accessory" domains from two toxins. Both truncated toxins exhibit significantly increased activity on purified ribosomes in vitro, suggesting one role of accessory domains is to reduce toxicity, which may help protect hosts from collateral damage. One of the truncated toxins also showed significantly reduced inactivation of cellular ribosomes in vivo, indicating a role for accessory domains in cell specificity. Together, these data reveal a mechanism for symbiont discrimination between hosts and parasites and highlight how dynamic toxin evolution can contribute to stability and novelty in defensive symbiosis.Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments. Many toxin-encoding bacteria have evolved into host-associated defensive partnerships, in which they use toxins to improve host survival during infection. The stability of these relationships requires that symbiont toxins target diverse parasites while minimizing damage to the host. We investigate the specificity of a group of ribosome-targeting toxins (RIPs) encoded by heritable Spiroplasma symbionts that contribute to defense against parasite infection in fruit fly hosts. Using E. coli to express five divergent copies of this toxin, we show that distantly related members of the family all retain the ability to inactivate ribosomes by adenine cleavage at the α-sarcin/ricin loop, the enzymatic hallmark of RIPs. However, when exposed to live insect and fungal cells, ribosome inactivation varies across the five toxins, suggesting cellular recognition or localization play a role in target specificity. To identify toxin domains required for specificity, we removed rapidly evolving "accessory" domains from two toxins. Both truncated toxins exhibit significantly increased activity on purified ribosomes in vitro, suggesting one role of accessory domains is to reduce toxicity, which may help protect hosts from collateral damage. One of the truncated toxins also showed significantly reduced inactivation of cellular ribosomes in vivo, indicating a role for accessory domains in cell specificity. Together, these data reveal a mechanism for symbiont discrimination between hosts and parasites and highlight how dynamic toxin evolution can contribute to stability and novelty in defensive symbiosis.
Author	Ballinger, Matthew J Moore, Logan D
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Copyright_xml	– notice: The Author(s) 2025. Published by Oxford University Press on behalf of the International Society for Microbial Ecology. – notice: The Author(s) 2025. Published by Oxford University Press on behalf of the International Society for Microbial Ecology. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2025 The Author(s) 2025. Published by Oxford University Press on behalf of the International Society for Microbial Ecology. This work is published under https://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet	Bacteria commonly deploy toxic proteins that act with specificity on target molecules to support invasion and improve survival in competitive environments....
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SubjectTerms	Adenine Animals Arthropods Arthropods - microbiology Bacteria Bacterial Toxins - genetics Bacterial Toxins - metabolism Biocompatibility Damage Deactivation E coli Escherichia coli - genetics Escherichia coli - metabolism Evolution Evolution, Molecular Insects Localization Parasites Proteins Ribonucleic acid Ribosome Inactivating Proteins - genetics Ribosome Inactivating Proteins - metabolism Ribosomes Ribosomes - drug effects Ribosomes - metabolism Ricin RNA Spiroplasma - genetics Spiroplasma - metabolism Spiroplasma - physiology Stability Survival Symbionts Symbiosis Toxicity Toxins
Title	Evolution of specialized toxin arsenals in a bacterial symbiont of arthropods
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