Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration
Coordination of diverse individuals often requires sophisticated communications and high-order computational abilities. Microbial populations can exhibit diverse individualistic behaviors, and yet can engage in collective migratory patterns with a spatially sorted arrangement of phenotypes. However,...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-11-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/67316 |
| _version_ | 1811199342159069184 |
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| author | Yang Bai Caiyun He Pan Chu Junjiajia Long Xuefei Li Xiongfei Fu |
| author_facet | Yang Bai Caiyun He Pan Chu Junjiajia Long Xuefei Li Xiongfei Fu |
| author_sort | Yang Bai |
| collection | DOAJ |
| description | Coordination of diverse individuals often requires sophisticated communications and high-order computational abilities. Microbial populations can exhibit diverse individualistic behaviors, and yet can engage in collective migratory patterns with a spatially sorted arrangement of phenotypes. However, it is unclear how such spatially sorted patterns emerge from diverse individuals without complex computational abilities. Here, by investigating the single-cell trajectories during group migration, we discovered that, despite the constant migrating speed of a group, the drift velocities of individual bacteria decrease from the back to the front. With a Langevin-type modeling framework, we showed that this decreasing profile of drift velocities implies the spatial modulation of individual run-and-tumble random motions, and enables the bacterial population to migrate as a pushed wave front. Theoretical analysis and stochastic simulations further predicted that the pushed wave front can help a diverse population to stay in a tight group, while diverse individuals perform the same type of mean reverting processes around centers orderly aligned by their chemotactic abilities. This mechanism about the emergence of orderly collective migration from diverse individuals is experimentally demonstrated by titration of bacterial chemoreceptor abundance. These results reveal a simple computational principle for emergent ordered behaviors from heterogeneous individuals. |
| first_indexed | 2024-04-12T01:46:29Z |
| format | Article |
| id | doaj.art-c455e94f3b914dbcb0de31da36890ffb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T01:46:29Z |
| publishDate | 2021-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c455e94f3b914dbcb0de31da36890ffb2022-12-22T03:53:04ZengeLife Sciences Publications LtdeLife2050-084X2021-11-011010.7554/eLife.67316Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migrationYang Bai0https://orcid.org/0000-0001-9976-2686Caiyun He1Pan Chu2Junjiajia Long3Xuefei Li4Xiongfei Fu5https://orcid.org/0000-0003-3657-8296CAS Key Laboratory for Quantitative Engineering Biology, Guangdong Provincial Key Laboratory of Synthetic Genomics, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory for Quantitative Engineering Biology, Guangdong Provincial Key Laboratory of Synthetic Genomics, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, ChinaCAS Key Laboratory for Quantitative Engineering Biology, Guangdong Provincial Key Laboratory of Synthetic Genomics, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, ChinaYale University, Department of Physics, New Haven, United StatesCAS Key Laboratory for Quantitative Engineering Biology, Guangdong Provincial Key Laboratory of Synthetic Genomics, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, ChinaCAS Key Laboratory for Quantitative Engineering Biology, Guangdong Provincial Key Laboratory of Synthetic Genomics, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, ChinaCoordination of diverse individuals often requires sophisticated communications and high-order computational abilities. Microbial populations can exhibit diverse individualistic behaviors, and yet can engage in collective migratory patterns with a spatially sorted arrangement of phenotypes. However, it is unclear how such spatially sorted patterns emerge from diverse individuals without complex computational abilities. Here, by investigating the single-cell trajectories during group migration, we discovered that, despite the constant migrating speed of a group, the drift velocities of individual bacteria decrease from the back to the front. With a Langevin-type modeling framework, we showed that this decreasing profile of drift velocities implies the spatial modulation of individual run-and-tumble random motions, and enables the bacterial population to migrate as a pushed wave front. Theoretical analysis and stochastic simulations further predicted that the pushed wave front can help a diverse population to stay in a tight group, while diverse individuals perform the same type of mean reverting processes around centers orderly aligned by their chemotactic abilities. This mechanism about the emergence of orderly collective migration from diverse individuals is experimentally demonstrated by titration of bacterial chemoreceptor abundance. These results reveal a simple computational principle for emergent ordered behaviors from heterogeneous individuals.https://elifesciences.org/articles/67316phenotypic diversitybacterial chemotaxiscollective behaviorpattern formationlangevin modelagent-based simulation |
| spellingShingle | Yang Bai Caiyun He Pan Chu Junjiajia Long Xuefei Li Xiongfei Fu Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration eLife phenotypic diversity bacterial chemotaxis collective behavior pattern formation langevin model agent-based simulation |
| title | Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| title_full | Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| title_fullStr | Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| title_full_unstemmed | Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| title_short | Spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| title_sort | spatial modulation of individual behaviors enables an ordered structure of diverse phenotypes during bacterial group migration |
| topic | phenotypic diversity bacterial chemotaxis collective behavior pattern formation langevin model agent-based simulation |
| url | https://elifesciences.org/articles/67316 |
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