In situ detection of ferric reductase activity in the intestinal lumen of an insect

Hernández-Gallardo, Anna Karen; Arcos-López, Trinidad; Bahena-Lopez, Jahir Marceliano; Tejeda-Guzmán, Carlos; Gallardo-Hernández, Salvador; Webb, Samuel M.; Kroll, Thomas; Solari, Pier Lorenzo; Sánchez-López, Carolina; Den Auwer, Christophe; Quintanar, Liliana; Missirlis, Fanis

doi:10.1007/s00775-024-02080-y

Title: In situ detection of ferric reductase activity in the intestinal lumen of an insect

Journal Article · 30 November 2024 · JBIC Journal of Biological Inorganic Chemistry

DOI: https://doi.org/10.1007/s00775-024-02080-y · OSTI ID:2481016

Hernández-Gallardo, Anna Karen ^[1];

^[1];

^[2]; Kroll, Thomas ^[2]; Solari, Pier Lorenzo ^[3];

^[1];

^[4];

^[1];

^[1]

Centro de Investigacion y de Estudios Avanzados (CINVESTAV), Mexico City (Mexico)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Synchrotron SOLEIL, Saint-Aubin (France)
Université Côte d’Azur, Nice (France)

The rise of atmospheric oxygen as a result of photosynthesis in cyanobacteria and chloroplasts has transformed most environmental iron into the ferric state. In contrast, cells within organisms maintain a reducing internal milieu and utilize predominantly ferrous iron. Ferric reductases are enzymes that transfer electrons to ferric ions, either extracellularly or within endocytic vesicles, enabling cellular ferrous iron uptake through Divalent Metal Transporter 1. In mammals, duodenal cytochrome b is a ferric reductase of the intestinal epithelium, but how insects reduce and absorb dietary iron remains unknown. Here we provide indirect evidence of extracellular ferric reductase activity in a small subset of Drosophila melanogaster intestinal epithelial cells, positioned at the neck of the midgut’s anterior region. Dietary-supplemented bathophenanthroline sulphate (BPS) captures locally generated ferrous iron and precipitates into pink granules, whose chemical identity was probed combining in situ X-ray absorption near edge structure and electron paramagnetic resonance spectroscopies. An increased presence of manganese ions upon BPS feeding was also found. Control animals were fed with ferric ammonium citrate, which is accumulated into ferritin iron in distinct intestinal subregions suggesting iron trafficking between different cells inside the animal. Spectroscopic signals from the biological samples were compared to purified Drosophila and horse spleen ferritin and to chemically synthesized BPS-iron and BPS-manganese complexes. The results corroborated the presence of BPS-iron in a newly identified ferric iron reductase region of the intestine, which we propose constitutes the major site of iron absorption in this organism.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: Conahcyt; National Institute of General Medical Sciences; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2481016

Journal Information:: JBIC Journal of Biological Inorganic Chemistry, Journal Name: JBIC Journal of Biological Inorganic Chemistry Journal Issue: 7-8 Vol. 29; ISSN 1432-1327

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Title: In situ detection of ferric reductase activity in the intestinal lumen of an insect

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