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Mol. Cells 2021; 44(8): 623-625

Published online August 31, 2021

https://doi.org/10.14348/molcells.2021.0201

© The Korean Society for Molecular and Cellular Biology

Eyeless Worms Can Run Away from Dangerous Blues

Caenorhabditis elegans without conventional eyes are equipped with a color-detecting system that helps in avoiding blue pathogenic bacteria.

Gee-Yoon Lee and Seung-Jae V. Lee*

Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, Korea

Correspondence to : seungjaevlee@kaist.ac.kr

Received: July 26, 2021; Accepted: August 4, 2021

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/.

The roundworm Caenorhabditis elegans is one of the most important model organisms for genetic research. Various environmental stimuli, including dietary cues and changes in ambient temperatures, affect the behavior and physiology of C. elegans (Goodman and Sengupta, 2019; Jeong et al., 2012). Interestingly, despite the lack of conventional eyes, C. elegans can perceive light via a signal transduction mechanism mediated by seven transmembrane receptors, including LITE-1 (high-energy LIghT unrEsponsive protein 1) (Gong et al., 2016; Iliff and Xu, 2020). Nevertheless, whether C. elegans can distinguish any color in the visible light, which was almost an unimaginable possibility, remained unknown.

Surprisingly, a recent study has reported that C. elegans can discriminate colors (Ghosh et al., 2021). They first tested whether C. elegans avoided harmful bacteria by detecting colored microbial pigments. Pseudomonas aeruginosa, a gram-negative opportunistic pathogenic bacterium in humans, is a popular model pathogen used for studying immunity and behavior of C. elegans (Park et al., 2017). P. aeruginosa secretes pyocyanin, a blue toxin that generates reactive oxygen species (ROS) (Mahajan-Miklos et al., 1999). C. elegans feeds on microbes enriched with potential pathogens in nature (Meisel and Kim, 2014; Schulenburg and Félix, 2017) and utilizes multiple sensory systems to avoid harmful bacteria (Meisel and Kim, 2014; Liu and Sun, 2021). Interestingly, Ghosh et al. (2021) demonstrated that C. elegans avoided P. aeruginosa better under white light than in the dark (Fig. 1). When exposed to a mutant P. aeruginosa strain that cannot synthesize pyocyanin, white light did not affect the avoidance behavior of C. elegans. In addition, C. elegans exhibited an increased avoidance to paraquat, a colorless ROS-generating toxin, only with blue dye or blue light, but did not avoid either paraquat or blue dye alone under white light. These data indicate that C. elegans avoids pyocyanin by perceiving both ROS and the blue color of the toxin (Fig. 1).

Can C. elegans discriminate among different colors to better avoid other adverse stimuli? The authors exposed C. elegans to the odor of 1-octanol, an aversive odorant, under different color combinations of blue-to-amber light. They found that colors ranging from blue to amber differentially affected its avoidance to 1-octanol, whereas exposure to pure blue or amber light had no effect on its avoidance to 1-octanol. Thus, C. elegans discriminates different colors of light to avoid aversive stimuli better.

Wild C. elegans lives in diverse natural habitats, including rotten fruits and soil, and encounters toxic microbes with various colors (Schulenburg and Félix, 2017). Thus, the authors tested whether C. elegans strains from various environmental niches responded differently to color combinations during foraging. Interestingly, several C. elegans strains displayed avoidance to colored light even without aversive stimuli. These results suggest that spectral sensitivity varies among wild C. elegans strains that live in different natural habitats.

To identify genetic factors responsible for variations in the color-dependent avoidance behaviors of C. elegans, the authors analyzed the genomes of 59 wild C. elegans strains. They found that single nucleotide variations in two cellular stress response genes of C. elegans, jkk-1 (c-Jun N-terminal kinase kinase 1) and lec-3 (galectin 3), were highly variable among the strains. The authors then showed that the genetic inhibition of jkk-1 or lec-3 in laboratory wild-type strains suppressed their color-dependent avoidance to 1-octanol. Overall, these results indicate that JKK-1 and LEC-3 are the key factors responsible for the color-dependent avoidance response of C. elegans (Fig. 1).

In summary, the authors showed that C. elegans, which do not have conventional eyes or color-detecting opsin receptors, can discriminate colors, and this trait is crucial for avoiding potentially harmful stimuli. They demonstrated that C. elegans that lives in various natural environments responds differently to colors and harmful odorants. This is the first report showing that C. elegans can distinguish among different colors of light by utilizing a newly discovered color-detecting system.

This ground-breaking work conducted by Ghosh et al. (2021) raises exciting possibilities regarding the evolution of color perception. C. elegans have been known to avoid ultraviolet light, and this study demonstrated that C. elegans avoids toxic bacteria via color perception. Many new questions arise from this study, as is the case for almost all the important discoveries. The color-detecting system in C. elegans may have evolutionarily emerged to avoid harmful stimuli for survival. If so, do C. elegans strains from different environmental niches avoid certain colors to enhance their survival in their own habitats? Do colors help C. elegans detect beneficial food sources as well? How do JKK-1 and LEC-3, which potentially play roles in cellular stress responses, mediate the color perception of C. elegans? In which neural circuits and molecular signaling pathways do JKK-1 and LEC-3 act? Do color-perceiving systems exist in other eyeless species, including mammals? Some mammals probably retain ancient color-detecting systems that may be utilized when their conventional visions are compromised. Addressing all these questions will help understand and devise novel biological systems that perceive colors without “seeing” them.

We thank all Lee laboratory members for helpful discussion and comments. This study is supported by the Korean Government (MSIT) through the National Research Foundation of Korea (NRF-2017R1A5A1015366) to S.J.V.L.

G.Y.L. and S.J.V.L. wrote the paper.

The authors have no potential conflicts of interest to disclose.

Fig. 1.C. elegans avoids toxic bacteria better by detecting blue color. P. aeruginosa, a pathogenic bacterium, synthesizes pyocyanin, a blue toxin that generates reactive oxygen species (ROS). C. elegans avoids blue color with ROS. JKK-1 (c-Jun N-terminal kinase kinase 1) and LEC-3 (galectin-3), which are cellular stress response proteins, mediate the blue color-dependent avoidance of wild-type C. elegans. This color detection system of C. elegans may help avoid pathogens and enhance its survival in nature.
  1. Ghosh D.D., Lee D., Jin X., Horvitz H.R., and Nitabach M.N. (2021). C. elegans discriminates colors to guide foraging. Science 371, 1059-1063.
    Pubmed CrossRef
  2. Gong J., Yuan Y., Ward A., Kang L., Zhang B., Wu Z., Peng J., Feng Z., Liu J., and Xu X.Z.S. (2016). The C. elegans taste receptor homolog LITE-1 is a photoreceptor. Cell 167, 1252-1263.e10.
    Pubmed CrossRef
  3. Goodman M.B. and Sengupta P. (2019). How Caenorhabditis elegans senses mechanical stress, temperature, and other physical stimuli. Genetics 212, 25-51.
    Pubmed KoreaMed CrossRef
  4. Iliff A.J. and Xu X.Z.S. (2020). C. elegans: a sensible model for sensory biology. J. Neurogenet. 34, 347-350.
    Pubmed KoreaMed CrossRef
  5. Jeong D.E., Artan M., Seo K., and Lee S.J. (2012). Regulation of lifespan by chemosensory and thermosensory systems: findings in invertebrates and their implications in mammalian aging. Front. Genet. 3, 218.
    Pubmed KoreaMed CrossRef
  6. Liu Y. and Sun J. (2021). Detection of pathogens and regulation of immunity by the Caenorhabditis elegans nervous system. mBio 12, e02301-20.
    Pubmed KoreaMed CrossRef
  7. Mahajan-Miklos S., Tan M.W., Rahme L.G., and Ausubel F.M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56.
    Pubmed CrossRef
  8. Meisel J.D. and Kim D.H. (2014). Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends Immunol. 35, 465-470.
    Pubmed CrossRef
  9. Park H.H., Jung Y., and Lee S.V. (2017). Survival assays using Caenorhabditis elegans. Mol. Cells 40, 90-99.
    Pubmed KoreaMed CrossRef
  10. Schulenburg H. and Félix M.A. (2017). The natural biotic environment of Caenorhabditis elegans. Genetics 206, 55-86.
    Pubmed KoreaMed CrossRef

Article

Journal Club

Mol. Cells 2021; 44(8): 623-625

Published online August 31, 2021 https://doi.org/10.14348/molcells.2021.0201

Copyright © The Korean Society for Molecular and Cellular Biology.

Eyeless Worms Can Run Away from Dangerous Blues

Caenorhabditis elegans without conventional eyes are equipped with a color-detecting system that helps in avoiding blue pathogenic bacteria.

Gee-Yoon Lee and Seung-Jae V. Lee*

Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, Korea

Correspondence to:seungjaevlee@kaist.ac.kr

Received: July 26, 2021; Accepted: August 4, 2021

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/.

Body

The roundworm Caenorhabditis elegans is one of the most important model organisms for genetic research. Various environmental stimuli, including dietary cues and changes in ambient temperatures, affect the behavior and physiology of C. elegans (Goodman and Sengupta, 2019; Jeong et al., 2012). Interestingly, despite the lack of conventional eyes, C. elegans can perceive light via a signal transduction mechanism mediated by seven transmembrane receptors, including LITE-1 (high-energy LIghT unrEsponsive protein 1) (Gong et al., 2016; Iliff and Xu, 2020). Nevertheless, whether C. elegans can distinguish any color in the visible light, which was almost an unimaginable possibility, remained unknown.

Surprisingly, a recent study has reported that C. elegans can discriminate colors (Ghosh et al., 2021). They first tested whether C. elegans avoided harmful bacteria by detecting colored microbial pigments. Pseudomonas aeruginosa, a gram-negative opportunistic pathogenic bacterium in humans, is a popular model pathogen used for studying immunity and behavior of C. elegans (Park et al., 2017). P. aeruginosa secretes pyocyanin, a blue toxin that generates reactive oxygen species (ROS) (Mahajan-Miklos et al., 1999). C. elegans feeds on microbes enriched with potential pathogens in nature (Meisel and Kim, 2014; Schulenburg and Félix, 2017) and utilizes multiple sensory systems to avoid harmful bacteria (Meisel and Kim, 2014; Liu and Sun, 2021). Interestingly, Ghosh et al. (2021) demonstrated that C. elegans avoided P. aeruginosa better under white light than in the dark (Fig. 1). When exposed to a mutant P. aeruginosa strain that cannot synthesize pyocyanin, white light did not affect the avoidance behavior of C. elegans. In addition, C. elegans exhibited an increased avoidance to paraquat, a colorless ROS-generating toxin, only with blue dye or blue light, but did not avoid either paraquat or blue dye alone under white light. These data indicate that C. elegans avoids pyocyanin by perceiving both ROS and the blue color of the toxin (Fig. 1).

Can C. elegans discriminate among different colors to better avoid other adverse stimuli? The authors exposed C. elegans to the odor of 1-octanol, an aversive odorant, under different color combinations of blue-to-amber light. They found that colors ranging from blue to amber differentially affected its avoidance to 1-octanol, whereas exposure to pure blue or amber light had no effect on its avoidance to 1-octanol. Thus, C. elegans discriminates different colors of light to avoid aversive stimuli better.

Wild C. elegans lives in diverse natural habitats, including rotten fruits and soil, and encounters toxic microbes with various colors (Schulenburg and Félix, 2017). Thus, the authors tested whether C. elegans strains from various environmental niches responded differently to color combinations during foraging. Interestingly, several C. elegans strains displayed avoidance to colored light even without aversive stimuli. These results suggest that spectral sensitivity varies among wild C. elegans strains that live in different natural habitats.

To identify genetic factors responsible for variations in the color-dependent avoidance behaviors of C. elegans, the authors analyzed the genomes of 59 wild C. elegans strains. They found that single nucleotide variations in two cellular stress response genes of C. elegans, jkk-1 (c-Jun N-terminal kinase kinase 1) and lec-3 (galectin 3), were highly variable among the strains. The authors then showed that the genetic inhibition of jkk-1 or lec-3 in laboratory wild-type strains suppressed their color-dependent avoidance to 1-octanol. Overall, these results indicate that JKK-1 and LEC-3 are the key factors responsible for the color-dependent avoidance response of C. elegans (Fig. 1).

In summary, the authors showed that C. elegans, which do not have conventional eyes or color-detecting opsin receptors, can discriminate colors, and this trait is crucial for avoiding potentially harmful stimuli. They demonstrated that C. elegans that lives in various natural environments responds differently to colors and harmful odorants. This is the first report showing that C. elegans can distinguish among different colors of light by utilizing a newly discovered color-detecting system.

This ground-breaking work conducted by Ghosh et al. (2021) raises exciting possibilities regarding the evolution of color perception. C. elegans have been known to avoid ultraviolet light, and this study demonstrated that C. elegans avoids toxic bacteria via color perception. Many new questions arise from this study, as is the case for almost all the important discoveries. The color-detecting system in C. elegans may have evolutionarily emerged to avoid harmful stimuli for survival. If so, do C. elegans strains from different environmental niches avoid certain colors to enhance their survival in their own habitats? Do colors help C. elegans detect beneficial food sources as well? How do JKK-1 and LEC-3, which potentially play roles in cellular stress responses, mediate the color perception of C. elegans? In which neural circuits and molecular signaling pathways do JKK-1 and LEC-3 act? Do color-perceiving systems exist in other eyeless species, including mammals? Some mammals probably retain ancient color-detecting systems that may be utilized when their conventional visions are compromised. Addressing all these questions will help understand and devise novel biological systems that perceive colors without “seeing” them.

ACKNOWLEDGMENTS

We thank all Lee laboratory members for helpful discussion and comments. This study is supported by the Korean Government (MSIT) through the National Research Foundation of Korea (NRF-2017R1A5A1015366) to S.J.V.L.

AUTHOR CONTRIBUTIONS

G.Y.L. and S.J.V.L. wrote the paper.

CONFLICT OF INTEREST

The authors have no potential conflicts of interest to disclose.

Fig. 1.C. elegans avoids toxic bacteria better by detecting blue color. P. aeruginosa, a pathogenic bacterium, synthesizes pyocyanin, a blue toxin that generates reactive oxygen species (ROS). C. elegans avoids blue color with ROS. JKK-1 (c-Jun N-terminal kinase kinase 1) and LEC-3 (galectin-3), which are cellular stress response proteins, mediate the blue color-dependent avoidance of wild-type C. elegans. This color detection system of C. elegans may help avoid pathogens and enhance its survival in nature.

Fig 1.

Figure 1.C. elegans avoids toxic bacteria better by detecting blue color. P. aeruginosa, a pathogenic bacterium, synthesizes pyocyanin, a blue toxin that generates reactive oxygen species (ROS). C. elegans avoids blue color with ROS. JKK-1 (c-Jun N-terminal kinase kinase 1) and LEC-3 (galectin-3), which are cellular stress response proteins, mediate the blue color-dependent avoidance of wild-type C. elegans. This color detection system of C. elegans may help avoid pathogens and enhance its survival in nature.
Molecules and Cells 2021; 44: 623-625https://doi.org/10.14348/molcells.2021.0201

References

  1. Ghosh D.D., Lee D., Jin X., Horvitz H.R., and Nitabach M.N. (2021). C. elegans discriminates colors to guide foraging. Science 371, 1059-1063.
    Pubmed CrossRef
  2. Gong J., Yuan Y., Ward A., Kang L., Zhang B., Wu Z., Peng J., Feng Z., Liu J., and Xu X.Z.S. (2016). The C. elegans taste receptor homolog LITE-1 is a photoreceptor. Cell 167, 1252-1263.e10.
    Pubmed CrossRef
  3. Goodman M.B. and Sengupta P. (2019). How Caenorhabditis elegans senses mechanical stress, temperature, and other physical stimuli. Genetics 212, 25-51.
    Pubmed KoreaMed CrossRef
  4. Iliff A.J. and Xu X.Z.S. (2020). C. elegans: a sensible model for sensory biology. J. Neurogenet. 34, 347-350.
    Pubmed KoreaMed CrossRef
  5. Jeong D.E., Artan M., Seo K., and Lee S.J. (2012). Regulation of lifespan by chemosensory and thermosensory systems: findings in invertebrates and their implications in mammalian aging. Front. Genet. 3, 218.
    Pubmed KoreaMed CrossRef
  6. Liu Y. and Sun J. (2021). Detection of pathogens and regulation of immunity by the Caenorhabditis elegans nervous system. mBio 12, e02301-20.
    Pubmed KoreaMed CrossRef
  7. Mahajan-Miklos S., Tan M.W., Rahme L.G., and Ausubel F.M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56.
    Pubmed CrossRef
  8. Meisel J.D. and Kim D.H. (2014). Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends Immunol. 35, 465-470.
    Pubmed CrossRef
  9. Park H.H., Jung Y., and Lee S.V. (2017). Survival assays using Caenorhabditis elegans. Mol. Cells 40, 90-99.
    Pubmed KoreaMed CrossRef
  10. Schulenburg H. and Félix M.A. (2017). The natural biotic environment of Caenorhabditis elegans. Genetics 206, 55-86.
    Pubmed KoreaMed CrossRef
Mol. Cells
Sep 30, 2021 Vol.44 No.9, pp. 627~698
COVER PICTURE
Non-mitochondrial localization of the N-terminal-deleted mutant form of ACSL1 in Cos7 cells. Green, ACSL1 mutant; Red, mitotracker; Blue, DAPI (Nan et al., pp. 637-646).

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