Cargando…

Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems

SIMPLE SUMMARY: Motile bacteria are widespread in various water ecosystems along with nonmotile species, which posits the question: what makes motility an advantage in such habitats, and under what conditions? This simulation study addresses these problems using a computer model of competition of tw...

Descripción completa

Detalles Bibliográficos
Autores principales: Klimenko, Alexandra, Matushkin, Yury, Kolchanov, Nikolay, Lashin, Sergey
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8533222/
https://www.ncbi.nlm.nih.gov/pubmed/34681118
http://dx.doi.org/10.3390/biology10101019
_version_ 1784587260739452928
author Klimenko, Alexandra
Matushkin, Yury
Kolchanov, Nikolay
Lashin, Sergey
author_facet Klimenko, Alexandra
Matushkin, Yury
Kolchanov, Nikolay
Lashin, Sergey
author_sort Klimenko, Alexandra
collection PubMed
description SIMPLE SUMMARY: Motile bacteria are widespread in various water ecosystems along with nonmotile species, which posits the question: what makes motility an advantage in such habitats, and under what conditions? This simulation study addresses these problems using a computer model of competition of two microbial species: Nomad of a motile population and Settler of a sedentary one. We simulated their competition under various environmental conditions such as the nutrient availability and frequency of changes in the location of the nutrient source as well as depending on some population parameters determining how much energy it takes for a bacterium to migrate and what the effect of density-dependent mortality is on the outcome of Settler vs. Nomad competition. We showed that dynamic and nutrient-scarce environments favour motile populations, whereas nutrient-rich and stagnant environments promote sedentary microorganisms. Moreover, the energetic costs of migration determine whether or not the motile population outcompetes the sedentary one, though it also depends on such conditions as nutrient availability. There is also another way for Settler to succeed even without penalties for migration—by grasping an opportunity to occupy the nutrient source, bringing about a biotic desert around it, which cannot be overcome by Nomad constantly searching for locally optimal conditions. ABSTRACT: Motility is a key adaptation factor in scarce marine environments inhabited by bacteria. The question of how a capacity for adaptive migrations influences the success of a microbial population in various conditions is a challenge addressed in this study. We employed the agent-based model of competition of motile and sedentary microbial populations in a confined aquatic environment supplied with a periodic batch nutrient source to assess the fitness of both. Such factors as nutrient concentration in a batch, batch period, mortality type and energetic costs of migration were considered to determine the conditions favouring different strategies: Nomad of a motile population and Settler of a sedentary one. The modelling results demonstrate that dynamic and nutrient-scarce environments favour motile populations, whereas nutrient-rich and stagnant environments promote sedentary microorganisms. Energetic costs of migration determine whether or not the Nomad strategy of the motile population is successful, though it also depends on such conditions as nutrient availability. Even without penalties for migration, under certain conditions, the sedentary Settler population dominates in the ecosystem. It is achieved by decreasing the local nutrient availability near the nutrient source, as motile populations relying on a local optimizing strategy tend to follow benign conditions and fail, enduring stress associated with crossing the valleys of suboptimal nutrient availability.
format Online
Article
Text
id pubmed-8533222
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-85332222021-10-23 Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems Klimenko, Alexandra Matushkin, Yury Kolchanov, Nikolay Lashin, Sergey Biology (Basel) Article SIMPLE SUMMARY: Motile bacteria are widespread in various water ecosystems along with nonmotile species, which posits the question: what makes motility an advantage in such habitats, and under what conditions? This simulation study addresses these problems using a computer model of competition of two microbial species: Nomad of a motile population and Settler of a sedentary one. We simulated their competition under various environmental conditions such as the nutrient availability and frequency of changes in the location of the nutrient source as well as depending on some population parameters determining how much energy it takes for a bacterium to migrate and what the effect of density-dependent mortality is on the outcome of Settler vs. Nomad competition. We showed that dynamic and nutrient-scarce environments favour motile populations, whereas nutrient-rich and stagnant environments promote sedentary microorganisms. Moreover, the energetic costs of migration determine whether or not the motile population outcompetes the sedentary one, though it also depends on such conditions as nutrient availability. There is also another way for Settler to succeed even without penalties for migration—by grasping an opportunity to occupy the nutrient source, bringing about a biotic desert around it, which cannot be overcome by Nomad constantly searching for locally optimal conditions. ABSTRACT: Motility is a key adaptation factor in scarce marine environments inhabited by bacteria. The question of how a capacity for adaptive migrations influences the success of a microbial population in various conditions is a challenge addressed in this study. We employed the agent-based model of competition of motile and sedentary microbial populations in a confined aquatic environment supplied with a periodic batch nutrient source to assess the fitness of both. Such factors as nutrient concentration in a batch, batch period, mortality type and energetic costs of migration were considered to determine the conditions favouring different strategies: Nomad of a motile population and Settler of a sedentary one. The modelling results demonstrate that dynamic and nutrient-scarce environments favour motile populations, whereas nutrient-rich and stagnant environments promote sedentary microorganisms. Energetic costs of migration determine whether or not the Nomad strategy of the motile population is successful, though it also depends on such conditions as nutrient availability. Even without penalties for migration, under certain conditions, the sedentary Settler population dominates in the ecosystem. It is achieved by decreasing the local nutrient availability near the nutrient source, as motile populations relying on a local optimizing strategy tend to follow benign conditions and fail, enduring stress associated with crossing the valleys of suboptimal nutrient availability. MDPI 2021-10-09 /pmc/articles/PMC8533222/ /pubmed/34681118 http://dx.doi.org/10.3390/biology10101019 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Klimenko, Alexandra
Matushkin, Yury
Kolchanov, Nikolay
Lashin, Sergey
Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title_full Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title_fullStr Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title_full_unstemmed Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title_short Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems
title_sort leave or stay: simulating motility and fitness of microorganisms in dynamic aquatic ecosystems
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8533222/
https://www.ncbi.nlm.nih.gov/pubmed/34681118
http://dx.doi.org/10.3390/biology10101019
work_keys_str_mv AT klimenkoalexandra leaveorstaysimulatingmotilityandfitnessofmicroorganismsindynamicaquaticecosystems
AT matushkinyury leaveorstaysimulatingmotilityandfitnessofmicroorganismsindynamicaquaticecosystems
AT kolchanovnikolay leaveorstaysimulatingmotilityandfitnessofmicroorganismsindynamicaquaticecosystems
AT lashinsergey leaveorstaysimulatingmotilityandfitnessofmicroorganismsindynamicaquaticecosystems