[en] [en] BACKGROUND: Shifts in dietary patterns during lifestyle transitions are integral components of the dynamic interactions between humans and their environments. Investigating the link between dietary diversity, the composition of the human lipidome and infection is key to understanding the interplay between diet and susceptibility to pathogens.
METHODS: Here we address this question by performing a comparative study of two ethnic groups with divergent dietary patterns: Fulani, who are nomad pastoralists with a dairy-centric diet, and Mossi, who are farmers with a plant-based diet. We generate 196 paired global lipidomes (927 lipid molecules) from both groups before and during natural Plasmodium falciparum infection.
RESULTS: Our analysis revealed 211 significantly differentially abundant lipid molecules between the two ethnic groups in both infection states. We show that ethnicity has a greater impact on the lipidome of these children than do P. falciparum infection and report inter-ethnic differences that impact pathogenesis. We highlight elevated levels of pentadecanoic acid (C15:0)-containing phospholipids in Fulani and experimentally demonstrate the suppressive effects of lysophosphatidylcholine LysoPC (15:0) on P. falciparum gametocyte production.
CONCLUSION: These findings link the Fulani's dairy-centric diet and lower P. falciparum gametocyte densities reported in this group and underscore the intricate links between dietary lipids and the host response to infection.
Disciplines :
Genetics & genetic processes
Author, co-author :
Abdrabou, Wael ; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Zorigt, Saruul; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Soulama, Issiaka; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso, Institut de Recherche en Sciences de la Santé, Ouagadougou, Burkina Faso
Bolatbay, Dariga ; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Dieng, Mame ; Université de Liège - ULiège > TERRA Research Centre ; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Jurkovic, Jakub ; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Sermé, Samuel Sindié; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
Sombié, Salif ; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
Henry, Noëlie Béré ; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
Kargougou, Désiré; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
Coulibaly, Sam Aboubacar; Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
Diawara, Aïssatou; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE
Idaghdour, Youssef ; Program in Biology, Division of Science, New York University Abu Dhabi, Abu Dhabi, UAE, Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, UAE. Electronic address: youssef.idaghdour@nyu.edu
This study was supported by the New York University Abu Dhabi funding grant (ADHPG AD105). We would like to express our gratitude to all participating Mossi and Fulani children, their families and community. We thank the staff of the Centre National de Recherche et de Formation sur le Paludisme for facilitating fieldwork in Burkina Faso. We thank Mostafa Khair (NYUAD Core Technology Platforms) for technical assistance, and Jane Carlton and Maria Nikulkova for their assistance to establish parasite culture protocols at NYUAD.
Bellwood, Peter, Early agriculturalist population diasporas? Farming, languages, and genes. Annu Rev Anthr 30:30 (2001), 181–207, 10.1146/ANNUREV.ANTHRO.30.1.181/CITE/REFWORKS.
Harrison, Genelle F., Sanz, Joaquin, Boulais, Jonathan, Mina, Michael J., Grenier, Jean Christophe, Leng, Yumei, et al. Natural selection contributed to immunological differences between hunter-gatherers and agriculturalists. Nat Ecol Evol 3:8 (2019), 1253–1264, 10.1038/s41559-019-0947-6.
Karlsson, Elinor K., Kwiatkowski, Dominic P., Sabeti, Pardis C., Natural selection and infectious disease in human populations. Nat Rev Genet 15:6 (2014), 379–393, 10.1038/NRG3734.
Alt, K.W., Al-Ahmad, A., Woelber, J.P., Nutrition and health in human evolution-past to present. Nutrients, 14(17), 2022, 3594, 10.3390/nu14173594.
Popkin, B.M., Nutritional patterns and transitions. Popul Dev Rev 19:1 (1993), 138–157, 10.2307/2938388.
Cassotta, Manuela, Forbes-Hernández, Tamara Yuliett, Iglesias, Ruben Calderón, Ruiz, Roberto, Zabaleta, Maria Elexpuru, Giampieri, Francesca, et al. Links between nutrition, infectious diseases, and microbiota: emerging technologies and opportunities for human-focused research. Nutrients 12:6 (2020), 1–28, 10.3390/NU12061827.
Kau, Andrew L., Ahern, Philip P., Griffin, Nicholas W., Goodman, Andrew L., Gordon, Jeffrey I., Human nutrition, the gut microbiome and the immune system. Nature 474:7351 (2011), 327–336, 10.1038/NATURE10213.
Yoon, Haejin, Shaw, Jillian L., Haigis, Marcia C., Greka, Anna, Lipid metabolism in sickness and in health: emerging regulators of lipotoxicity. Mol Cell 81:18 (2021), 3708–3730, 10.1016/J.MOLCEL.2021.08.027.
Laishram Dolie, D., Sutton Patrick, L., Nutan, Nanda, Sharma Vijay, L., Sobti Ranbir, C., Carlton Jane, M., et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J 11:1 (2012), 1–15, 10.1186/1475-2875-11-29/TABLES/1.
Gulati, Sonia, Ekland, Eric H., Ruggles, Kelly V., Marti, Matthias, Paolo, Gilbert Di, Fidock, David A., Profiling the essential nature of lipid metabolism in asexual blood and gametocyte stages of Plasmodium falciparum correspondence. Cell Host Microbe 18 (2015), 371–381, 10.1016/j.chom.2015.08.003.
Kilian, Nicole, Choi, Jae Yeon, Voelker, Dennis R., Mamoun, Choukri Ben, Role of phospholipid synthesis in the development and differentiation of malaria parasites in the blood. J Biol Chem, 293(45), 2018, 17308, 10.1074/JBC.R118.003213.
Nikulkova, Maria, Abdrabou, Wael, Carlton, Jane M., Idaghdour, Youssef, Exploiting integrative metabolomics to study host–parasite interactions in Plasmodium infections. Trends Parasitol 40:4 (2024), 313–323, 10.1016/j.pt.2024.02.007.
Filarsky, Michael, Fraschka, Sabine A., Niederwieser, Igor, Brancucci, Nicolas M.B., Carrington, Eilidh, Carrió, Elvira, et al. GDV1 induces sexual commitment of malaria parasites by antagonizing HP1-dependent gene silencing. Science, 359(6381), 2018, 1259, 10.1126/SCIENCE.AAN6042.
Brancucci, Nicolas M.B., Bertschi, Nicole L., Zhu, Lei, Niederwieser, Igor, Chin, Wai Hoe, Wampfler, Rahel, et al. Heterochromatin protein 1 secures survival and transmission of malaria parasites. Cell Host Microbe 16:2 (2014), 165–176, 10.1016/j.chom.2014.07.004.
Meibalan, E., Marti, M., Biology of Malaria Transmission. Cold Spring Harb Perspect Med, 7(3), 2017, a025452, 10.1101/cshperspect.a025452.
Tran, P.N., Brown, S.H.J., Rug, M., Ridgway, M.C., Mitchell, T.W., Maier, A.G., Changes in lipid composition during sexual development of the malaria parasite Plasmodium falciparum. Malar J, 15, 2016, 73, 10.1186/s12936-016-1130-z.
Brancucci, Nicolas M.B., Gerdt, Joseph P., Wang, Cheng Qi, De Niz, Mariana, Philip, Nisha, Adapa, Swamy R., et al. Lysophosphatidylcholine regulates sexual stage differentiation in the human malaria parasite Plasmodium falciparum. Cell 171:7 (2017), 1532–1544.e15, 10.1016/j.cell.2017.10.020.
Zuzarte-Luís, Vanessa, Mello-Vieira, João, Marreiros, Inês M., Liehl, Peter, Chora, Ângelo F., Carret, C.éline K., et al. Dietary alterations modulate susceptibility to Plasmodium infection. Nat Microbiol 2:12 (2017), 1600–1607, 10.1038/s41564-017-0025-2.
Dolo, Amagana, Modiano, David, Maiga, Boubacar, Daou, Modibo, Dolo, Guimogo, Guindo, Hamadoun, et al. Difference in susceptibility to malaria between two sympatric ethnic groups in Mali. Am J Trop Med Hyg 72:3 (2005), 243–248, 10.4269/ajtmh.2005.72.243.
Modiano, D., Petrarca, V., Sirima, B.S., Nebié, I., Diallo, D., Esposito, F., et al. Different response to Plasmodium falciparum malaria in West African sympatric ethnic groups. Proc Natl Acad Sci USA 93:23 (1996), 13206–13211, 10.1073/pnas.93.23.13206.
Troye-Blomberg, Marita, Arama, Charles, Quin, Jaclyn, Bujila, Ioana, Östlund Farrants, Ann Kristin, What will studies of Fulani individuals naturally exposed to malaria teach us about protective immunity to malaria?. Scand J Immunol 92:4 (2020), 1–7, 10.1111/sji.12932.
Lykke, Anne Mette, Mertz, Ole, Ganaba, Souleymane, Food consumption in rural Burkina Faso. Ecol Food Nutr 41:2 (2002), 119–153, 10.1080/03670240214492.
Turner, Matthew D., Teague, Molly, Ayantunde, Augustine, Eating groups within households: differentiation in food consumption by age, gender, and genealogical position in rural Burkina Faso. Food Policy, 101, 2021, 102093, 10.1016/J.FOODPOL.2021.102093.
Casari, S., Di Paola, M., Banci, E., et al. Changing dietary habits: the impact of urbanization and rising socio-economic status in families from Burkina Faso in Sub-Saharan Africa. Nutrients, 14(9), 2022, 1782, 10.3390/nu14091782.
Becquey, Elodie, Savy, Mathilde, Danel, Peggy, Dabiré, Hubert B., Tapsoba, Sylvestre, Martin-Prével, Yves, Dietary patterns of adults living in Ouagadougou and their association with overweight. Nutr J, 9(1), 2010, 13, 10.1186/1475-2891-9-13.
De Filippo, Carlotta, Cavalieri, Duccio, Di Paola, Monica, Ramazzotti, Matteo, Poullet, Jean Baptiste, Massart, Sebastien, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:33 (2010), 14691–14696, 10.1073/PNAS.1005963107/SUPPL_FILE/PNAS.201005963SI.PDF.
Boström, Stéphanie, Giusti, Pablo, Arama, Charles, Persson, Jan Olov, Dara, Victor, Traore, Boubacar, et al. Changes in the levels of cytokines, chemokines and malaria-specific antibodies in response to Plasmodium falciparum infection in children living in sympatry in Mali. Malar J, 11(1), 2012, 109, 10.1186/1475-2875-11-109.
Portugal, Silvia, Doumtabe, Didier, Traore, Boubacar, Miller, Louis H., Troye-Blomberg, Marita, Doumbo, Ogobara K., et al. B cell analysis of ethnic groups in Mali with differential susceptibility to malaria. Malar J, 11(1), 2012, 162, 10.1186/1475-2875-11-162.
Abdrabou, Wael, Dieng, Mame Massar, Diawara, A.ïssatou, Sermé, Samuel Sindié, Almojil, Dareen, Sombié, Salif, et al. Metabolome modulation of the host adaptive immunity in human malaria. Nat Metab 3:7 (2021), 1001–1016, 10.1038/s42255-021-00404-9.
Bereczky, Sandor, Dolo, A., Maiga, B., Hayano, M., Granath, F., Montgomery, S.M., et al. Spleen enlargement and genetic diversity of Plasmodium falciparum infection in two ethnic groups with different malaria susceptibility in Mali, West Africa. Trans R Soc Trop Med Hyg 100:3 (2006), 248–257, 10.1016/j.trstmh.2005.03.011.
Paganotti, G.M., Palladino, C., Modiano, D., Sirima, B.S., Råberg, L., Diarra, A., et al. Genetic complexity and gametocyte production of Plasmodium falciparum in Fulani and Mossi communities in Burkina Faso. Parasitology 132:5 (2006), 607–614, 10.1017/S0031182005009601.
Casari, S, Di Paola, M, Banci, E, Diallo, S., Scarallo, L., Renzo, S., et al. Changing dietary habits: the impact of urbanization and rising socio-economic status in families from Burkina Faso in Sub-Saharan Africa. Nutrients, 14(9), 2022, 1782, 10.3390/nu14091782.
Löfgren, Lars, Ståhlman, Marcus, Forsberg, Gun Britt, Saarinen, Sinikka, Nilsson, Ralf, Hansson, Gor̈an I., The BUME method: a novel automated chloroform-free 96-well total lipid extraction method for blood plasma. J Lipid Res 53:8 (2012), 1690–1700, 10.1194/jlr.D023036.
Freinkman E, Evans AM. A Technical Guide to Metabolon's Complex Lipids Targeted Panel. Metabolon, Inc.; 2023. Available at: https://www.metabolon.com/wp-content/uploads/2023/07/Metabolon-Whitepaper-Complex-Lipids-Targeted-Panel-2.pdf. Accessed November 3, 2024.
Lambros Chris, Vandenberg Jerome P. Synchronization of Plasmodium falciparum Erythrocytic Stages in Culture. Author(s): Chris Lambros and Jerome P. Vanderberg Published by: Allen Press on behalf of The American Society of Parasitologists Stable URL: https://www.jstor.org/stable/3280287. Journal Parasitology 1979;65(3):418–20.
Lambros, C., Vanderberg, J.P., Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:3 (1979), 418–420, 10.2307/3280287.
Brancucci, Nicolas M.B., Goldowitz, Ilana, Buchholz, Kathrin, Werling, Kristine, Marti, Matthias, An assay to probe Plasmodium falciparum growth, transmission stage formation and early gametocyte development. Nat Protoc 10:8 (2015), 1131–1142, 10.1038/nprot.2015.072.
Moll Kirsten, Kaneko Akira, Scherf Arthur, Wahlgren Mats. Methods in Malaria Research 6th Edition; 2013.
Venn-Watson, Stephanie, Schork, Nicholas J., Pentadecanoic acid (C15:0), an essential fatty acid, shares clinically relevant cell-based activities with leading longevity-enhancing compounds. Nutrients, 15(21), 2023, 4607, 10.3390/NU15214607/S1.
Venn-Watson, S.K., Butterworth, C.N., Broader and safer clinically-relevant activities of pentadecanoic acid compared to omega-3: evaluation of an emerging essential fatty acid across twelve primary human cell-based disease systems. PLoS One, 17(5), 2022, e0268778, 10.1371/journal.pone.0268778.
Venn-Watson, Stephanie, Lumpkin, Richard, Dennis, Edward A., Efficacy of dietary odd-chain saturated fatty acid pentadecanoic acid parallels broad associated health benefits in humans: could it be essential?. Sci Rep 10:1 (2020), 1–14, 10.1038/s41598-020-64960-y.
Brevik, Asgeir, Veierød, M.B., Drevon, C.A., Andersen, L.F., Evaluation of the odd fatty acids 15:0 and 17:0 in serum and adipose tissue as markers of intake of milk and dairy fat. Eur J Clin Nutr 59:12 (2005), 1417–1422, 10.1038/sj.ejcn.1602256.
Jenkins, Benjamin, West, James A., Koulman, Albert, A review of odd-chain fatty acid metabolism and the role of pentadecanoic acid (C15:0) and heptadecanoic acid (C17:0) in health and disease. Molecules 20:2 (2015), 2425–2444, 10.3390/MOLECULES20022425.
Quehenberger, Oswald, Dennis, Edward A., The human plasma lipidome. N Engl J Med, 365(19), 2011, 1812, 10.1056/NEJMRA1104901.
Trieu, Kathy, Bhat, Saiuj, Dai, Zhaoli, Leander, Karin, Gigante, Bruna, Qian, Frank, et al. Biomarkers of dairy fat intake, incident cardiovascular disease, and all-cause mortality: a cohort study, systematic review, and meta-analysis. PLoS Med, 18(9), 2021, e1003763, 10.1371/JOURNAL.PMED.1003763.
Golley, Rebecca K., Hendrie, Gilly A., Evaluation of the relative concentration of serum fatty acids C14:0, C15:0 and C17:0 as markers of children's dairy fat intake. Ann Nutr Metab 65:4 (2014), 310–316, 10.1159/000368325.
Brevik, Asgeir, Veierød, M.B., Drevon, C.A., Andersen, L.F., Evaluation of the odd fatty acids 15:0 and 17:0 in serum and adipose tissue as markers of intake of milk and dairy fat. Eur J Clin Nutr 59:12 (2005), 1417–1422, 10.1038/sj.ejcn.1602256.
Jenkins, Benjamin, Aoun, Manar, Feillet-Coudray, Christine, Coudray, Charles, Ronis, Martin, Koulman, Albert, The dietary total-fat content affects the in vivo circulating C15:0 and C17:0 fatty acid levels independently. Nutrients, 10(11), 2018, 1646, 10.3390/NU10111646.
Santaren, Ingrid D., Watkins, Steven M., Liese, Angela D., Wagenknecht, Lynne E., Rewers, Marian J., Haffner, Steven M., et al. Serum pentadecanoic acid (15:0), a short-term marker of dairy food intake, is inversely associated with incident type 2 diabetes and its underlying disorders. Am J Clin Nutr, 100(6), 2014, 1532, 10.3945/AJCN.114.092544.
Huang, Lihua, Lin, Jie Sheng, Aris, Izzuddin M., Yang, Guiyou, Chen, Wei Qing, Li, Ling Jun, Circulating saturated fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Nutrients, 11(5), 2019, 998, 10.3390/NU11050998.
Khaw, Kay Tee, Friesen, Marlin D., Riboli, Elio, Luben, Robert, Wareham, Nicholas, Plasma phospholipid fatty acid concentration and incident coronary heart disease in men and women: the EPIC-Norfolk prospective study. PLoS Med, 9(7), 2012, e1001255, 10.1371/JOURNAL.PMED.1001255.
Unger, Allison L., Torres-Gonzalez, Moises, Kraft, Jana, Dairy fat consumption and the risk of metabolic syndrome: an examination of the saturated fatty acids in dairy. Nutrients, 11(9), 2019, 2200, 10.3390/NU11092200.
Matejcic, M., Lesueur, F., Biessy, C., Renault, A.L., Mebirouk, N., Yammine, S., et al. Circulating plasma phospholipid fatty acids and risk of pancreatic cancer in a large European cohort. Int J Cancer 143:10 (2018), 2437–2448, 10.1002/IJC.31797.
Hellgren, L.I., Nordby, P., Bioactive lipids in dairy fat,. Watson, R.R., Collier, R.J., Preedy, V.R., (eds.) Dairy in Human Health and Disease Across the Lifespan, 2017, Academic Press, 233–237, 10.1016/B978-0-12-809868-4.00017-0.
Chowdhury, R., Steur, M., Patel, P.S., Franco, O.H., Individual fatty acids in cardiometabolic disease. Watson, R.R., De Meester, F., (eds.) Handbook of Lipids in Human Function: Fatty Acids, 2016, Academic Press and AOCS Press, 207–318, 10.1016/B978-1-63067-036-8.00010-X.
Trieu, Kathy, Bhat, Saiuj, Dai, Zhaoli, Leander, Karin, Gigante, Bruna, Qian, Frank, et al. Biomarkers of dairy fat intake, incident cardiovascular disease, and all-cause mortality: a cohort study, systematic review, and meta-analysis. PLoS Med, 18(9), 2021, e1003763, 10.1371/JOURNAL.PMED.1003763.
Stewart, L.B., Freville, A., Voss, T.S., Baker, D.A., Awandare, G.A., Conway, D.J., Plasmodium falciparum sexual commitment rate variation among clinical isolates and diverse laboratory-adapted lines. Microbiol Spectr 10:6 (2022), e02234–22, 10.1128/spectrum.02234-22.
Venugopal, Kannan, Hentzschel, Franziska, Valkiūnas, Gediminas, Marti, Matthias, Plasmodium asexual growth and sexual development in the haematopoietic niche of the host. Nat Rev Microbiol 18:3 (2020), 177–189, 10.1038/s41579-019-0306-2.
Brancucci, N.M.B., De Niz, M., Straub, T.J., et al. Probing Plasmodium falciparum sexual commitment at the single-cell level. Wellcome Open Res, 3, 2018, 70, 10.12688/wellcomeopenres.14645.4.
Harris, Chantal T., Tong, Xinran, Campelo, Riward, Marreiros, Inês M., Vanheer, Leen N., Nahiyaan, Navid, et al. Sexual differentiation in human malaria parasites is regulated by competition between phospholipid metabolism and histone methylation. Nat Microbiol 8:7 (2023), 1280–1292, 10.1038/s41564-023-01396-w.
