Hongfei Chen , Tom Hata , Ricardo Cortez , Hoa Nguyen , M.A.R. Koehl , Lisa Fauci
{"title":"A new optimized regularized Stokeslet model reveals the effects of multicellular protozoan colony configuration on hydrodynamic performance","authors":"Hongfei Chen , Tom Hata , Ricardo Cortez , Hoa Nguyen , M.A.R. Koehl , Lisa Fauci","doi":"10.1016/j.mbs.2025.109519","DOIUrl":null,"url":null,"abstract":"<div><div>Many microbial eukaryotes have unicellular life stages, but can also form multicellular colonies. We explored hydrodynamic consequences of colony morphology, which affects swimming and flux of prey-carrying water to cells in a colony, using the choanoflagellate, <em>Choanoeca flexa</em>, which forms cup-like colonies that can turn inside-out so flagella line the cup’s interior or cover its outside surface. Detailed hydrodynamic models incorporating cell morphologies are not feasible for colonies with many cells. Therefore, we designed a reduced model of each cell using regularized-force-dipoles with parameters optimized (by selecting the regularized delta function from a given class) to match the flow-field of a detailed model of a cell. Calculated swimming speeds and water flux to flagella-in colonies match those measured for living <em>C. flexa</em>. For a given shape (flat bowls, hemispheres, spherical cups) of flagella-in colony, models showed that swimming speed and water flux towards the colony increases with cell density, although flux per cell is independent of density. Denser packing of cells at the front of flagella-in colonies increases swimming speed and flux to cells at all positions in the colonies. Flagella-in colonies swim more slowly, but produce higher water flux per cell than do flagella-out colonies of the same configuration, suggesting that flagella-out colonies are better swimmers, whereas flagella-in colonies are better feeders. A model flagella-out colony with morphology matched to a real <em>C. flexa</em> requires a flagellar force 5–10 times greater than that for flagella-in colonies to achieve the measured swimming speed, suggesting flagella beat differently on flagella-out colonies.</div></div>","PeriodicalId":51119,"journal":{"name":"Mathematical Biosciences","volume":"389 ","pages":"Article 109519"},"PeriodicalIF":1.8000,"publicationDate":"2025-08-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Mathematical Biosciences","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0025556425001452","RegionNum":4,"RegionCategory":"数学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Many microbial eukaryotes have unicellular life stages, but can also form multicellular colonies. We explored hydrodynamic consequences of colony morphology, which affects swimming and flux of prey-carrying water to cells in a colony, using the choanoflagellate, Choanoeca flexa, which forms cup-like colonies that can turn inside-out so flagella line the cup’s interior or cover its outside surface. Detailed hydrodynamic models incorporating cell morphologies are not feasible for colonies with many cells. Therefore, we designed a reduced model of each cell using regularized-force-dipoles with parameters optimized (by selecting the regularized delta function from a given class) to match the flow-field of a detailed model of a cell. Calculated swimming speeds and water flux to flagella-in colonies match those measured for living C. flexa. For a given shape (flat bowls, hemispheres, spherical cups) of flagella-in colony, models showed that swimming speed and water flux towards the colony increases with cell density, although flux per cell is independent of density. Denser packing of cells at the front of flagella-in colonies increases swimming speed and flux to cells at all positions in the colonies. Flagella-in colonies swim more slowly, but produce higher water flux per cell than do flagella-out colonies of the same configuration, suggesting that flagella-out colonies are better swimmers, whereas flagella-in colonies are better feeders. A model flagella-out colony with morphology matched to a real C. flexa requires a flagellar force 5–10 times greater than that for flagella-in colonies to achieve the measured swimming speed, suggesting flagella beat differently on flagella-out colonies.
期刊介绍:
Mathematical Biosciences publishes work providing new concepts or new understanding of biological systems using mathematical models, or methodological articles likely to find application to multiple biological systems. Papers are expected to present a major research finding of broad significance for the biological sciences, or mathematical biology. Mathematical Biosciences welcomes original research articles, letters, reviews and perspectives.