Details

Autor(en) / Beteiligte

• García-Lozano, Marleny
• Henzler, Christine
• Porras, Miguel Ángel González
• Pons, Inès
• Berasategui, Aileen
• Lanz, Christa
• Budde, Heike
• Oguchi, Kohei
• Matsuura, Yu
• Pauchet, Yannick
• Goffredi, Shana
• Fukatsu, Takema
• Windsor, Donald
• Salem, Hassan

Titel

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Ist Teil von

• Current biology, 2024-04, Vol.34 (8), p.1621-1634.e9

Ort / Verlag

England: Elsevier Inc

Erscheinungsjahr

2024

Quelle

Elsevier ScienceDirect Journals

Beschreibungen/Notizen

• Timing the acquisition of a beneficial microbe relative to the evolutionary history of its host can shed light on the adaptive impact of a partnership. Here, we investigated the onset and molecular evolution of an obligate symbiosis between Cassidinae leaf beetles and Candidatus Stammera capleta, a γ-proteobacterium. Residing extracellularly within foregut symbiotic organs, Stammera upgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe that Stammera is a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. In contrast to its transcriptional profile during vertical transmission, Stammera elevates the expression of genes encoding digestive enzymes while in the foregut symbiotic organs, matching the nutritional requirements of its host. Despite the widespread distribution of Stammera across Cassidinae beetles, symbiont acquisition during the Paleocene (∼62 mya) did not coincide with the origin of the subfamily. Early diverging lineages lack the symbiont and the specialized organs that house it. Reconstructing the ancestral state of host-beneficial factors revealed that Stammera encoded three digestive enzymes at the onset of symbiosis, including polygalacturonase—a pectinase that is universally shared. Although non-symbiotic cassidines encode polygalacturonase endogenously, their repertoire of plant cell wall-degrading enzymes is more limited compared with symbiotic beetles supplemented with digestive enzymes from Stammera. Highlighting the potential impact of a symbiotic condition and an upgraded metabolic potential, Stammera-harboring beetles exploit a greater variety of plants and are more speciose compared with non-symbiotic members of the Cassidinae. [Display omitted] •Stammera is a shared symbiont across tortoise and hispine leaf beetles•Stammera modulates its transcriptional profile to match host requirements•The digestive symbiosis originated in the Paleocene (62 mya)•Symbiotic beetles are more speciose than their non-symbiotic relatives García-Lozano et al. time the acquisition and quantify the adaptive impact of a digestive symbiosis between leaf beetles and Stammera, a bacterium. Compared with their non-symbiotic relatives, Stammera-harboring leaf beetles deploy a greater variety of digestive enzymes, exploit a broader range of plants, and are more speciose.