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ISME J., Jan 08 2024, 18 (1) wrad021 | https://doi.org/10.1093/ismejo/wrad021
Specialized digestive mechanism for an insect-bacterium gut symbiosis
Junbeom Lee 1, Bohyun Jeong 2, Jeongtae Kim 3, Jae H Cho 4, Jin H Byeon 4, Bok L Lee 4, Jiyeun K Kim 2
1Metabolomics Research Center for Functional Materials, Kyungsung University, Busan 48434, South Korea.
2Department of Microbiology, Kosin University College of Medicine, Busan 49267, South Korea.
3Department of Anatomy, Kosin University College of Medicine, Busan 49267, South Korea.
4Host Defense Protein Laboratory, College of Pharmacy, Pusan National University, Busan 46241, South Korea.
Corresponding author: Jiyeun K. Kim
Abstract
In Burkholderia-Riptortus symbiosis, the host bean bug Riptortus pedestris harbors Burkholderia symbionts in its symbiotic organ, M4 midgut, for use as a nutrient source. After occupying M4, excess Burkholderia symbionts are moved to the M4B region, wherein they are effectively digested and absorbed. Previous studies have shown that M4B has strong symbiont-specific antibacterial activity, which is not because of the expression of antimicrobial peptides but rather because of the expression of digestive enzymes, mainly cathepsin L protease. However, in this study, inhibition of cathepsin L activity did not reduce the bactericidal activity of M4B, indicating that there is an unknown digestive mechanism that renders specifically potent bactericidal activity against Burkholderia symbionts. Transmission electron microscopy revealed that the lumen of symbiotic M4B was filled with a fibrillar matter in contrast to the empty lumen of aposymbiotic M4B. Using chromatographic and electrophoretic analyses, we found that the bactericidal substances in M4B existed as high-molecular-weight (HMW) complexes that were resistant to protease degradation. The bactericidal HMW complexes were visualized on non-denaturing gels using protein- and polysaccharide-staining reagents, thereby indicating that the HMW complexes are composed of proteins and polysaccharides. Strongly stained M4B lumen with Periodic acid-Schiff (PAS) reagent in M4B paraffin sections confirmed HMW complexes with polysaccharide components. Furthermore, M4B smears stained with Periodic acid-Schiff revealed the presence of polysaccharide fibers. Therefore, we propose a key digestive mechanism of M4B: bacteriolytic fibers, polysaccharide fibers associated with digestive enzymes such as cathepsin L, specialized for Burkholderia symbionts in Riptortus gut symbiosis.
논문정보
- Research article
- 2024년 01월 (BRIC 등록일 2024-02-20)
- 국내 연구진
- 의약학 > 감염의학
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