Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence
The opportunistic pathogen Pseudomonas aeruginosa is ubiquitous in the environment, and in humans, it is capable of causing acute or chronic infections. In the natural environment, predation by bacterivorous protozoa represents a primary threat to bacteria. Here, we determined the impact of long-ter...
| Main Authors: | , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Journal Article |
| Language: | English |
| Published: |
2022
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| Online Access: | https://hdl.handle.net/10356/160067 |
| _version_ | 1811692291765567488 |
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| author | Leong, Wai Poh, Wee Han Williams, Jonathan Lutz, Carla Hoque, M. Mozammel Poh, Yan Hong Yee, Benny Yeo Ken Chua, Cliff Givskov, Michael Sanderson-Smith, Martina Rice, Scott A. McDougald, Diane |
| author2 | School of Biological Sciences |
| author_facet | School of Biological Sciences Leong, Wai Poh, Wee Han Williams, Jonathan Lutz, Carla Hoque, M. Mozammel Poh, Yan Hong Yee, Benny Yeo Ken Chua, Cliff Givskov, Michael Sanderson-Smith, Martina Rice, Scott A. McDougald, Diane |
| author_sort | Leong, Wai |
| collection | NTU |
| description | The opportunistic pathogen Pseudomonas aeruginosa is ubiquitous in the environment, and in humans, it is capable of causing acute or chronic infections. In the natural environment, predation by bacterivorous protozoa represents a primary threat to bacteria. Here, we determined the impact of long-term exposure of P. aeruginosa to predation pressure. P. aeruginosa persisted when coincubated with the bacterivorous Acanthamoeba castellanii for extended periods and produced genetic and phenotypic variants. Sequencing of late-stage amoeba-adapted P. aeruginosa isolates demonstrated single nucleotide polymorphisms within genes that encode known virulence factors, and this correlated with a reduction in expression of virulence traits. Virulence for the nematode Caenorhabditis elegans was attenuated in late-stage amoeba-adapted P. aeruginosa compared to early-stage amoeba-adapted and nonadapted counterparts. Further, late-stage amoeba-adapted P. aeruginosa showed increased competitive fitness and enhanced survival in amoebae as well as in macrophage and neutrophils. Interestingly, our findings indicate that the selection imposed by amoebae resulted in P. aeruginosa isolates with reduced virulence and enhanced fitness, similar to those recovered from chronic cystic fibrosis infections. Thus, predation by protozoa and long-term colonization of the human host may represent similar environments that select for similar losses of gene function. IMPORTANCE Pseudomonas aeruginosa is an opportunistic pathogen that causes both acute infections in plants and animals, including humans, and chronic infections in immunocompromised and cystic fibrosis patients. This bacterium is commonly found in soils and water, where bacteria are constantly under threat of being consumed by bacterial predators, e.g., protozoa. To escape being killed, bacteria have evolved a suite of mechanisms that protect them from being consumed or digested. Here, we examined the effect of long-term predation on the genotypes and phenotypes expressed by P. aeruginosa. We show that long-term coincubation with protozoa gave rise to mutations that resulted in P. aeruginosa becoming less pathogenic. This is particularly interesting as similar mutations arise in bacteria associated with chronic infections. Importantly, the genetic and phenotypic traits possessed by late-stage amoeba-adapted P. aeruginosa are similar to those observed in isolates obtained from chronic cystic fibrosis infections. This notable overlap in adaptation to different host types suggests similar selection pressures among host cell types as well as similar adaptation strategies. |
| first_indexed | 2024-10-01T06:33:27Z |
| format | Journal Article |
| id | ntu-10356/160067 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T06:33:27Z |
| publishDate | 2022 |
| record_format | dspace |
| spelling | ntu-10356/1600672022-07-16T20:11:51Z Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence Leong, Wai Poh, Wee Han Williams, Jonathan Lutz, Carla Hoque, M. Mozammel Poh, Yan Hong Yee, Benny Yeo Ken Chua, Cliff Givskov, Michael Sanderson-Smith, Martina Rice, Scott A. McDougald, Diane School of Biological Sciences Singapore Centre for Environmental Life Sciences and Engineering (SCELSE) Science::Biological sciences Pseudomonas Biofilm The opportunistic pathogen Pseudomonas aeruginosa is ubiquitous in the environment, and in humans, it is capable of causing acute or chronic infections. In the natural environment, predation by bacterivorous protozoa represents a primary threat to bacteria. Here, we determined the impact of long-term exposure of P. aeruginosa to predation pressure. P. aeruginosa persisted when coincubated with the bacterivorous Acanthamoeba castellanii for extended periods and produced genetic and phenotypic variants. Sequencing of late-stage amoeba-adapted P. aeruginosa isolates demonstrated single nucleotide polymorphisms within genes that encode known virulence factors, and this correlated with a reduction in expression of virulence traits. Virulence for the nematode Caenorhabditis elegans was attenuated in late-stage amoeba-adapted P. aeruginosa compared to early-stage amoeba-adapted and nonadapted counterparts. Further, late-stage amoeba-adapted P. aeruginosa showed increased competitive fitness and enhanced survival in amoebae as well as in macrophage and neutrophils. Interestingly, our findings indicate that the selection imposed by amoebae resulted in P. aeruginosa isolates with reduced virulence and enhanced fitness, similar to those recovered from chronic cystic fibrosis infections. Thus, predation by protozoa and long-term colonization of the human host may represent similar environments that select for similar losses of gene function. IMPORTANCE Pseudomonas aeruginosa is an opportunistic pathogen that causes both acute infections in plants and animals, including humans, and chronic infections in immunocompromised and cystic fibrosis patients. This bacterium is commonly found in soils and water, where bacteria are constantly under threat of being consumed by bacterial predators, e.g., protozoa. To escape being killed, bacteria have evolved a suite of mechanisms that protect them from being consumed or digested. Here, we examined the effect of long-term predation on the genotypes and phenotypes expressed by P. aeruginosa. We show that long-term coincubation with protozoa gave rise to mutations that resulted in P. aeruginosa becoming less pathogenic. This is particularly interesting as similar mutations arise in bacteria associated with chronic infections. Importantly, the genetic and phenotypic traits possessed by late-stage amoeba-adapted P. aeruginosa are similar to those observed in isolates obtained from chronic cystic fibrosis infections. This notable overlap in adaptation to different host types suggests similar selection pressures among host cell types as well as similar adaptation strategies. Ministry of Education (MOE) National Research Foundation (NRF) Published version We acknowledge support from the iThree Institute at the University of Technology Sydney, Sydney, Australia, from the Australian Research Council Discovery Project (DP170100453), and from the National Research Foundation and Ministry of Education Singapore under its Research Centre of Excellence Program to the Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University. 2022-07-12T05:42:08Z 2022-07-12T05:42:08Z 2022 Journal Article Leong, W., Poh, W. H., Williams, J., Lutz, C., Hoque, M. M., Poh, Y. H., Yee, B. Y. K., Chua, C., Givskov, M., Sanderson-Smith, M., Rice, S. A. & McDougald, D. (2022). Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence. Applied and Environmental Microbiology, 88(5), e02322-21-. https://dx.doi.org/10.1128/aem.02322-21 0099-2240 https://hdl.handle.net/10356/160067 10.1128/aem.02322-21 35020451 2-s2.0-85126072793 5 88 e02322-21 en Applied and Environmental Microbiology © 2022 Leong et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. application/pdf |
| spellingShingle | Science::Biological sciences Pseudomonas Biofilm Leong, Wai Poh, Wee Han Williams, Jonathan Lutz, Carla Hoque, M. Mozammel Poh, Yan Hong Yee, Benny Yeo Ken Chua, Cliff Givskov, Michael Sanderson-Smith, Martina Rice, Scott A. McDougald, Diane Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title | Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title_full | Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title_fullStr | Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title_full_unstemmed | Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title_short | Adaptation to an amoeba host leads to Pseudomonas aeruginosa isolates with attenuated virulence |
| title_sort | adaptation to an amoeba host leads to pseudomonas aeruginosa isolates with attenuated virulence |
| topic | Science::Biological sciences Pseudomonas Biofilm |
| url | https://hdl.handle.net/10356/160067 |
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