Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system
Abstract Quantifying virulence remains a central problem in human health, pest control, disease ecology, and evolutionary biology. Bacterial virulence is typically quantified by the LT50 (i.e., the time taken to kill 50% of infected hosts); however, such an indicator cannot account for the full comp...
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| Format: | Article |
| Language: | English |
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Springer Nature
2019-06-01
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| Series: | Molecular Systems Biology |
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| Online Access: | https://doi.org/10.15252/msb.20188707 |
| _version_ | 1797282508801310720 |
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| author | Tommaso Biancalani Jeff Gore |
| author_facet | Tommaso Biancalani Jeff Gore |
| author_sort | Tommaso Biancalani |
| collection | DOAJ |
| description | Abstract Quantifying virulence remains a central problem in human health, pest control, disease ecology, and evolutionary biology. Bacterial virulence is typically quantified by the LT50 (i.e., the time taken to kill 50% of infected hosts); however, such an indicator cannot account for the full complexity of the infection process, such as distinguishing between the pathogen's ability to colonize versus kill the hosts. Indeed, the pathogen needs to breach the primary defenses in order to colonize, find a suitable environment to replicate, and finally express the virulence factors that cause disease. Here, we show that two virulence attributes, namely pathogen lethality and invasiveness, can be disentangled from the survival curves of a laboratory population of Caenorhabditis elegans nematodes exposed to three bacterial pathogens: Pseudomonas aeruginosa, Serratia marcescens, and Salmonella enterica. We first show that the host population eventually experiences a constant mortality rate, which quantifies the lethality of the pathogen. We then show that the time necessary to reach this constant mortality rate regime depends on the pathogen growth rate and colonization rate, and thus determines the pathogen invasiveness. Our framework reveals that Serratia marcescens is particularly good at the initial colonization of the host, whereas Salmonella enterica is a poor colonizer yet just as lethal once established. Pseudomonas aeruginosa, on the other hand, is both a good colonizer and highly lethal after becoming established. The ability to quantitatively characterize the ability of different pathogens to perform each of these steps has implications for treatment and prevention of disease and for the evolution and ecology of pathogens. |
| first_indexed | 2024-03-07T17:15:03Z |
| format | Article |
| id | doaj.art-9f19c72bfbbf4808b7c2030193baac6e |
| institution | Directory Open Access Journal |
| issn | 1744-4292 |
| language | English |
| last_indexed | 2024-03-07T17:15:03Z |
| publishDate | 2019-06-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj.art-9f19c72bfbbf4808b7c2030193baac6e2024-03-02T23:29:01ZengSpringer NatureMolecular Systems Biology1744-42922019-06-01156n/an/a10.15252/msb.20188707Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen systemTommaso Biancalani0Jeff Gore1Physics of Living Systems Department of Physics Massachusetts Institute of Technology Cambridge MA USAPhysics of Living Systems Department of Physics Massachusetts Institute of Technology Cambridge MA USAAbstract Quantifying virulence remains a central problem in human health, pest control, disease ecology, and evolutionary biology. Bacterial virulence is typically quantified by the LT50 (i.e., the time taken to kill 50% of infected hosts); however, such an indicator cannot account for the full complexity of the infection process, such as distinguishing between the pathogen's ability to colonize versus kill the hosts. Indeed, the pathogen needs to breach the primary defenses in order to colonize, find a suitable environment to replicate, and finally express the virulence factors that cause disease. Here, we show that two virulence attributes, namely pathogen lethality and invasiveness, can be disentangled from the survival curves of a laboratory population of Caenorhabditis elegans nematodes exposed to three bacterial pathogens: Pseudomonas aeruginosa, Serratia marcescens, and Salmonella enterica. We first show that the host population eventually experiences a constant mortality rate, which quantifies the lethality of the pathogen. We then show that the time necessary to reach this constant mortality rate regime depends on the pathogen growth rate and colonization rate, and thus determines the pathogen invasiveness. Our framework reveals that Serratia marcescens is particularly good at the initial colonization of the host, whereas Salmonella enterica is a poor colonizer yet just as lethal once established. Pseudomonas aeruginosa, on the other hand, is both a good colonizer and highly lethal after becoming established. The ability to quantitatively characterize the ability of different pathogens to perform each of these steps has implications for treatment and prevention of disease and for the evolution and ecology of pathogens.https://doi.org/10.15252/msb.20188707C. eleganshost–pathogenmicrobial ecologypopulation dynamicsvirulence |
| spellingShingle | Tommaso Biancalani Jeff Gore Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system Molecular Systems Biology C. elegans host–pathogen microbial ecology population dynamics virulence |
| title | Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system |
| title_full | Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system |
| title_fullStr | Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system |
| title_full_unstemmed | Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system |
| title_short | Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system |
| title_sort | disentangling bacterial invasiveness from lethality in an experimental host pathogen system |
| topic | C. elegans host–pathogen microbial ecology population dynamics virulence |
| url | https://doi.org/10.15252/msb.20188707 |
| work_keys_str_mv | AT tommasobiancalani disentanglingbacterialinvasivenessfromlethalityinanexperimentalhostpathogensystem AT jeffgore disentanglingbacterialinvasivenessfromlethalityinanexperimentalhostpathogensystem |