Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
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
_version_ 1784710527873712128
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
work_keys_str_mv AT sieksmeyerthorben eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT heshulin eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT esparzamoramalejandra eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT jiangshixiong eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT petrasiunaitevesta eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT kuropkabenno eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT banasiakronald eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT julsethmarajean eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT weisechristoph eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT johnstonpaulr eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT rodriguezrojasalexandro eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis
AT mcmahondinop eatinginalosingcauselimitedbenefitofmodifiedmacronutrientconsumptionfollowinginfectionintheorientalcockroachblattaorientalis