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Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis
BACKGROUND: Host–pathogen interactions can lead to dramatic changes in host feeding behaviour. One aspect of this includes self-medication, where infected individuals consume substances such as toxins or alter their macronutrient consumption to enhance immune competence. Another widely adopted anima...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118584/ https://www.ncbi.nlm.nih.gov/pubmed/35585501 http://dx.doi.org/10.1186/s12862-022-02007-8 |
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author | Sieksmeyer, Thorben He, Shulin Esparza-Mora, M. Alejandra Jiang, Shixiong Petrašiūnaitė, Vesta Kuropka, Benno Banasiak, Ronald Julseth, Mara Jean Weise, Christoph Johnston, Paul R. Rodríguez-Rojas, Alexandro McMahon, Dino P. |
author_facet | Sieksmeyer, Thorben He, Shulin Esparza-Mora, M. Alejandra Jiang, Shixiong Petrašiūnaitė, Vesta Kuropka, Benno Banasiak, Ronald Julseth, Mara Jean Weise, Christoph Johnston, Paul R. Rodríguez-Rojas, Alexandro McMahon, Dino P. |
author_sort | Sieksmeyer, Thorben |
collection | PubMed |
description | BACKGROUND: Host–pathogen interactions can lead to dramatic changes in host feeding behaviour. One aspect of this includes self-medication, where infected individuals consume substances such as toxins or alter their macronutrient consumption to enhance immune competence. Another widely adopted animal response to infection is illness-induced anorexia, which is thought to assist host immunity directly or by limiting the nutritional resources available to pathogens. Here, we recorded macronutrient preferences of the global pest cockroach, Blatta orientalis to investigate how shifts in host macronutrient dietary preference and quantity of carbohydrate (C) and protein (P) interact with immunity following bacterial infection. RESULTS: We find that B. orientalis avoids diets enriched for P under normal conditions, and that high P diets reduce cockroach survival in the long term. However, following bacterial challenge, cockroaches significantly reduced their overall nutrient intake, particularly of carbohydrates, and increased the relative ratio of protein (P:C) consumed. Surprisingly, these behavioural shifts had a limited effect on cockroach immunity and survival, with minor changes to immune protein abundance and antimicrobial activity between individuals placed on different diets, regardless of infection status. CONCLUSIONS: We show that cockroach feeding behaviour can be modulated by a pathogen, resulting in an illness-induced anorexia-like feeding response and a shift from a C-enriched to a more P:C equal diet. However, our results also indicate that such responses do not provide significant immune protection in B. orientalis, suggesting that the host’s dietary shift might also result from random rather than directed behaviour. The lack of an apparent benefit of the shift in feeding behaviour highlights a possible reduced importance of diet in immune regulation in these invasive animals, although further investigations employing pathogens with alternative infection strategies are warranted. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02007-8. |
format | Online Article Text |
id | pubmed-9118584 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91185842022-05-20 Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis Sieksmeyer, Thorben He, Shulin Esparza-Mora, M. Alejandra Jiang, Shixiong Petrašiūnaitė, Vesta Kuropka, Benno Banasiak, Ronald Julseth, Mara Jean Weise, Christoph Johnston, Paul R. Rodríguez-Rojas, Alexandro McMahon, Dino P. BMC Ecol Evol Research Article BACKGROUND: Host–pathogen interactions can lead to dramatic changes in host feeding behaviour. One aspect of this includes self-medication, where infected individuals consume substances such as toxins or alter their macronutrient consumption to enhance immune competence. Another widely adopted animal response to infection is illness-induced anorexia, which is thought to assist host immunity directly or by limiting the nutritional resources available to pathogens. Here, we recorded macronutrient preferences of the global pest cockroach, Blatta orientalis to investigate how shifts in host macronutrient dietary preference and quantity of carbohydrate (C) and protein (P) interact with immunity following bacterial infection. RESULTS: We find that B. orientalis avoids diets enriched for P under normal conditions, and that high P diets reduce cockroach survival in the long term. However, following bacterial challenge, cockroaches significantly reduced their overall nutrient intake, particularly of carbohydrates, and increased the relative ratio of protein (P:C) consumed. Surprisingly, these behavioural shifts had a limited effect on cockroach immunity and survival, with minor changes to immune protein abundance and antimicrobial activity between individuals placed on different diets, regardless of infection status. CONCLUSIONS: We show that cockroach feeding behaviour can be modulated by a pathogen, resulting in an illness-induced anorexia-like feeding response and a shift from a C-enriched to a more P:C equal diet. However, our results also indicate that such responses do not provide significant immune protection in B. orientalis, suggesting that the host’s dietary shift might also result from random rather than directed behaviour. The lack of an apparent benefit of the shift in feeding behaviour highlights a possible reduced importance of diet in immune regulation in these invasive animals, although further investigations employing pathogens with alternative infection strategies are warranted. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02007-8. BioMed Central 2022-05-18 /pmc/articles/PMC9118584/ /pubmed/35585501 http://dx.doi.org/10.1186/s12862-022-02007-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Sieksmeyer, Thorben He, Shulin Esparza-Mora, M. Alejandra Jiang, Shixiong Petrašiūnaitė, Vesta Kuropka, Benno Banasiak, Ronald Julseth, Mara Jean Weise, Christoph Johnston, Paul R. Rodríguez-Rojas, Alexandro McMahon, Dino P. Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title | Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title_full | Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title_fullStr | Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title_full_unstemmed | Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title_short | Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis |
title_sort | eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach blatta orientalis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118584/ https://www.ncbi.nlm.nih.gov/pubmed/35585501 http://dx.doi.org/10.1186/s12862-022-02007-8 |
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