Spiroplasma in Glossina fuscipes fuscipes: a potential manipulator of male reproduction
5 affiliations
- 1Department of Biology and Biotechnology “Lazzaro Spallanzani”, University of Pavia, Pavia, Italy
- 2Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, Connecticut, USA
- 3Insect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, Vienna, Austria
- 4Institute of Molecular Genetics (IGM), Italian National Research Council (CNR), Pavia, Italy
- 5Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
Abstract
Glossina fuscipes fuscipes (Gff) is a riverine species of the Glossina genus (tsetse flies). It is one of the principal vector species responsible for transmitting human African trypanosomiasis across a broad swath of sub-Saharan Africa. Consequently, it remains a primary target for vector-control interventions in endemic regions. As with other Glossina species, G. fuscipes houses a highly streamlined microbiota, composed of maternally transmitted endosymbionts mandatory for survival, which also significantly impacts the vectorial capacity. Among them, the obligate Wigglesworthia provides essential nutrients and stimulates maturation of the fly’s immune system, providing a refractory effect against Trypanosoma. It also harbors the commensal Sodalis and parasitic Wolbachia, the latter of which induces cytoplasmic incompatibility. In addition, Gff hosts a Spiroplasma strain that enhances host refractoriness to trypanosome infection but disrupts female metabolic and reproductive homeostasis. We used high-throughput RNA sequencing to examine the impact of Spiroplasma on male testes and accessory glands to reveal how this microbe exerts its influence on male reproductive physiology. We found that Spiroplasma substantially alters testes physiology, downregulating genes involved in energy metabolism and sperm function, suggesting reduced male reproductive fitness. In contrast, accessory gland gene expression was not significantly affected despite the critical role of these organs in semen production and reproductive success, considering also that the bacterium exploits the ejaculate to further increase its population prevalence. Spiroplasma infection also correlated with increased abundance of other symbionts, including Wigglesworthia.
IMPORTANCE: A complex host-symbiont interplay makes the Spiroplasma harbored in tsetse fly intriguing. The unexpected male-specific energetic costs of Spiroplasma infection keep open the biological question of why this bacterium is maintained in this species. On the other hand, Spiroplasma infection correlates with increased abundance of Wigglesworthia, promoting trypanosome refractoriness. The present work adds a valuable layer to further interpret the ecological and evolutionary narrative of Spiroplasma interactions, and lays the preliminary groundwork to explore the potential of using Spiroplasma as a biocontrol agent. While acknowledging that our findings were derived from a long-established laboratory colony, the data on the modulation of fly reproductive fitness and on the possible contribution to trypanosome refractoriness found make Spiroplasma intriguing for strategic integration into environmentally sustainable vector management programs, potentially in concert with the Sterile Insect Technique. The results provide significant advances in symbiont-host interactions, bringing new insight into understanding the role of symbionts in viviparous tsetse flies. We also provide a community forum for discussion on the possible use of bacteria as species-specific biocontrol.
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BibTeX
@article{piccinno2026spiroplasma,
title = {{Spiroplasma in Glossina fuscipes fuscipes: a potential manipulator of male reproduction}},
author = {Riccardo Piccinno and Giulia Fiorenza and Francesco Lescai and Simone Carpanzano and Fabian Gstöttenmayer and Kiswend-sida M. Dera and Anna Cleta Croce and Chantel J. de Beer and Brian L. Weiss and Mariangela Santorsola and Alberta Pinnola and Giuliano Gasperi and Federico Forneris and Serap Aksoy and Adly M. M. Abd-Alla and Anna Rodolfa Malacrida},
journal = {mSystems},
year = {2026},
month = sep,
doi = {10.1128/msystems.00526-26},
url = {https://doi.org/10.1128/msystems.00526-26},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Spiroplasma in Glossina fuscipes fuscipes: a potential manipulator of male reproduction
AU - Riccardo Piccinno
AU - Giulia Fiorenza
AU - Francesco Lescai
AU - Simone Carpanzano
AU - Fabian Gstöttenmayer
AU - Kiswend-sida M. Dera
AU - Anna Cleta Croce
AU - Chantel J. de Beer
AU - Brian L. Weiss
AU - Mariangela Santorsola
AU - Alberta Pinnola
AU - Giuliano Gasperi
AU - Federico Forneris
AU - Serap Aksoy
AU - Adly M. M. Abd-Alla
AU - Anna Rodolfa Malacrida
PY - 2026
DA - 2026/09/11
JO - mSystems
DO - 10.1128/msystems.00526-26
UR - https://doi.org/10.1128/msystems.00526-26
AB - Glossina fuscipes fuscipes (Gff) is a riverine species of the Glossina genus (tsetse flies). It is one of the principal vector species responsible for transmitting human African trypanosomiasis across a broad swath of sub-Saharan Africa. Consequently, it remains a primary target for vector-control interventions in endemic regions. As with other Glossina species, G. fuscipes houses a highly streamlined microbiota, composed of maternally transmitted endosymbionts mandatory for survival, which also significantly impacts the vectorial capacity. Among them, the obligate Wigglesworthia provides essential nutrients and stimulates maturation of the fly’s immune system, providing a refractory effect against Trypanosoma. It also harbors the commensal Sodalis and parasitic Wolbachia, the latter of which induces cytoplasmic incompatibility. In addition, Gff hosts a Spiroplasma strain that enhances host refractoriness to trypanosome infection but disrupts female metabolic and reproductive homeostasis. We used high-throughput RNA sequencing to examine the impact of Spiroplasma on male testes and accessory glands to reveal how this microbe exerts its influence on male reproductive physiology. We found that Spiroplasma substantially alters testes physiology, downregulating genes involved in energy metabolism and sperm function, suggesting reduced male reproductive fitness. In contrast, accessory gland gene expression was not significantly affected despite the critical role of these organs in semen production and reproductive success, considering also that the bacterium exploits the ejaculate to further increase its population prevalence. Spiroplasma infection also correlated with increased abundance of other symbionts, including Wigglesworthia. IMPORTANCE: A complex host-symbiont interplay makes the Spiroplasma harbored in tsetse fly intriguing. The unexpected male-specific energetic costs of Spiroplasma infection keep open the biological question of why this bacterium is maintained in this species. On the other hand, Spiroplasma infection correlates with increased abundance of Wigglesworthia, promoting trypanosome refractoriness. The present work adds a valuable layer to further interpret the ecological and evolutionary narrative of Spiroplasma interactions, and lays the preliminary groundwork to explore the potential of using Spiroplasma as a biocontrol agent. While acknowledging that our findings were derived from a long-established laboratory colony, the data on the modulation of fly reproductive fitness and on the possible contribution to trypanosome refractoriness found make Spiroplasma intriguing for strategic integration into environmentally sustainable vector management programs, potentially in concert with the Sterile Insect Technique. The results provide significant advances in symbiont-host interactions, bringing new insight into understanding the role of symbionts in viviparous tsetse flies. We also provide a community forum for discussion on the possible use of bacteria as species-specific biocontrol.
SN - 2379-5077
ER -