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Subcellular niche segregation of co-obligate symbionts in whiteflies

View ORCID ProfileAkiko Fujiwara, Xian-Ying Meng, View ORCID ProfileYoichi Kamagata, View ORCID ProfileTsutomu Tsuchida
doi: https://doi.org/10.1101/2022.11.18.517168
Akiko Fujiwara
aCenter for Food Science and Wellness, Gunma University, Maebashi 371-8510, Japan
bChemical Genomics Research Group, RIKEN Center for Sustainable Resource Science, Wako, 351-0198, Japan
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Xian-Ying Meng
cBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan
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Yoichi Kamagata
cBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan
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Tsutomu Tsuchida
dFaculty of Science, Academic Assembly, University of Toyama, 3190 Gofuku, Toyama City, Toyama, 930-8555, Japan
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  • For correspondence: tsuchida@sci.u-toyama.ac.jp
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Abstract

Many insects contain endosymbiotic bacteria within their bodies. In multiple endosymbiotic systems comprising two or more symbionts, each of the symbionts is generally localized in a different host cell or tissue. Bemisia tabaci (Sweet potato whitefly)possesses a unique endosymbiotic system where co-obligate symbionts are localized in the same bacteriocytes. Using fluorescence in situ hybridization, we found that endosymbionts in B. tabaci MEAM1 occupy distinct subcellular habitats, or niches, within a single bacteriocyte. Hamiltonella was located adjacent to the nucleus of the bacteriocyte, while Portiera was present in the cytoplasm surrounding Hamiltonella. Immunohistochemical analysis revealed that the endoplasmic reticulum separates the two symbionts. Habitat segregation was maintained for longer durations in female bacteriocytes. The same segregation was observed in three genetically distinct B. tabaci groups (MEAM1, MED Q1, and Asia II 6) and Trialeurodes vaporariorum, which shared a common ancestor with Bemisia over 80 million years ago, even though the coexisting symbionts and the size of bacteriocytes were different. These results suggest that the habitat segregation system existed in the common ancestor and was conserved in both lineages, despite different bacterial partners coexisting with Portiera. Our findings provide insights into the evolution and maintenance of complex endosymbiotic systems and highlight the importance of organelles for the construction of separate niches for endosymbionts.

Importance Co-obligate endosymbionts in B. tabaci are exceptionally localized within the same bacteriocyte (a specialized cell for endosymbiosis), but the underlying mechanism for their coexistence remains largely unknown. This study provides evidence for niche segregation at the subcellular level between the two symbionts. We showed that the endoplasmic reticulum is a physical barrier separating the two species. Despite differences in co-obligate partners, this subcellular niche segregation was conserved across various whitefly species. The physical proximity of symbionts may enable the efficient biosynthesis of essential nutrients via shared metabolic pathways. The expression “Good fences make good neighbors” appears to be true for insect endosymbiotic systems.

Competing Interest Statement

The authors have declared no competing interest.

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Posted November 19, 2022.
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Subcellular niche segregation of co-obligate symbionts in whiteflies
Akiko Fujiwara, Xian-Ying Meng, Yoichi Kamagata, Tsutomu Tsuchida
bioRxiv 2022.11.18.517168; doi: https://doi.org/10.1101/2022.11.18.517168
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Subcellular niche segregation of co-obligate symbionts in whiteflies
Akiko Fujiwara, Xian-Ying Meng, Yoichi Kamagata, Tsutomu Tsuchida
bioRxiv 2022.11.18.517168; doi: https://doi.org/10.1101/2022.11.18.517168

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