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For centuries, humans have cultivated cannabis for the pharmacological properties that result from consuming its specialized metabolites, primarily cannabinoids and terpenoids. Today, cannabis is a multi-billion-dollar industry whose existence rests on the biological activity of tiny cell clusters, called glandular trichomes, found mainly on flowers. Cannabinoids are toxic to cannabis cells,1 and how the trichome cells can produce and secrete massive quantities of lipophilic metabolites is not known. 1 To address this gap in knowledge, we investigated cannabis glandular trichomes using ultra-rapid cryofixation, quantitative electron microscopy, and immuno-gold labeling of cannabinoid pathway enzymes. We demonstrate that the metabolically active cells in cannabis form a "supercell," with extensive cytoplasmic bridges across the cell walls and a polar distribution of organelles adjacent to the apical surface where metabolites are secreted. The predicted metabolic role of the non-photosynthetic plastids is supported by unusual membrane arrays in the plastids and the localization of the start of the cannabinoid/terpene pathway in the stroma of the plastids. Abundant membrane contact sites connected plastid paracrystalline cores with the plastid envelope, plastid with endoplasmic reticulum (ER), and ER with plasma membrane. The final step of cannabinoid biosynthesis, catalyzed by tetrahydrocannabinolic acid synthase (THCAS), was localized in the cell-surface wall facing the extracellular storage cavity. We propose a new model of how the cannabis cells can support abundant metabolite production, with emphasis on the key role of membrane contact sites and extracellular THCA biosynthesis. This new model can inform synthetic biology approaches for cannabinoid production in yeast or cell cultures. • Glandular cells form a polarized syncytium during THCA production and secretion • GPPS is located in plastids that contain conspicuous membrane fusions • THCAS is located exclusively on the extracellular surface of trichomes • Membrane contacts among plastids, ER, and PM inform a new trafficking model Cannabinoids and terpenes are biosynthesized, secreted, and stored in cannabis glandular trichomes. Livingston et al. reveal the nanoscale distribution of the enzymes involved in cannabinoid biosynthesis and the unique cellular environment where these enzymes operate. A new model of metabolite trafficking from the plastid to the cell wall is proposed. [ABSTRACT FROM AUTHOR]

Coral reefs are a biodiversity hotspot, 1,2 and the association between coral and intracellular dinoflagellates is a model for endosymbiosis. 3,4 Recently, corals and related anthozoans have also been found to harbor another kind of endosymbiont, apicomplexans called corallicolids. 5 Apicomplexans are a diverse lineage of obligate intracellular parasites 6 that include human pathogens such as the malaria parasite, Plasmodium. 7 Global environmental sequencing shows corallicolids are tightly associated with tropical and subtropical reef environments, 5,8,9 where they infect diverse corals across a range of depths in many reef systems, and correlate with host mortality during bleaching events. 10 All of this points to corallicolids being ecologically significant to coral reefs, but it is also possible they are even more widely distributed because most environmental sampling is biased against parasites that maintain a tight association with their hosts throughout their life cycle. We tested the global distribution of corallicolids using a more direct approach, by specifically targeting potential anthozoan host animals from cold/temperate marine waters outside the coral reef context. We found that corallicolids are in fact common in such hosts, in some cases at high frequency, and that they infect the same tissue as parasites from topical coral reefs. Parasite phylogeny suggests corallicolids move between hosts and habitats relatively frequently, but that biogeography is more conserved. Overall, these results greatly expand the range of corallicolids beyond coral reefs, suggesting they are globally distributed parasites of marine anthozoans, which also illustrates significant blind spots that result from strategies commonly used to sample microbial biodiversity. • Coral parasites are found in cold-water ecosystems • They infect animals related to corals, such as anemones and corallimorphs • Biogeography is a major factor in parasite evolution • Current strategies for sampling microbial diversity overlook important parasites Corallicolids are coral parasites that were thought to be restricted to coral reef ecosystems. Trznadel et al. show that they are widely distributed, infecting related hosts, such as anemones, in cold marine environments. This shows that corallicolids are globally relevant parasites and raises questions about biases in microbial diversity surveys. [ABSTRACT FROM AUTHOR]