Predation in a Microbial World: Mechanisms and Trade-Offs of Flagellate Foraging

Literature Cited

1. Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL et al. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66:4–119
   [Google Scholar]
2. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D et al. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:429–514
   [Google Scholar]
3. Andersen A, Kiørboe T. 2020. The effect of tethering on the clearance rate of suspension-feeding plankton. PNAS 117:30101–3
   [Google Scholar]
4. Andersen A, Wadhwa N, Kiørboe T. 2015. Quiet swimming at low Reynolds number. Phys. Rev. E 91:042712
   [Google Scholar]
5. Andersen P. 1988. Functional biology of the choanoflagellate Diaphanoeca grandis Ellis. Mar. Microb. Food Webs 3:235–50
   [Google Scholar]
6. Asadzadeh SS, Nielsen LT, Andersen A, Dölger J, Kiørboe T et al. 2019. Hydrodynamic functionality of the lorica in choanoflagellates. J. R. Soc. Interface 16:20180478
   [Google Scholar]
7. Asadzadeh SS, Walther JH, Andersen A, Kiørboe T. 2022. Hydrodynamic interactions are key in thrust-generation of hairy flagella. Phys. Rev. Fluids 7:073101
   [Google Scholar]
8. Berdach JT. 1977. In situ preservation of the transverse flagellum of Peridinium cinctum (Dinophyceae) for scanning electron microscopy. J. Phycol. 13:243–51
   [Google Scholar]
9. Berggreen U, Hansen B, Kiørboe T. 1988. Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar. Biol. 99:341–52
   [Google Scholar]
10. Blom JF, Horňák K, Šimek K, Pernthaler J. 2010. Aggregate formation in a freshwater bacterial strain induced by growth state and conspecific chemical cues. Environ. Microbiol. 12:2486–95
    [Google Scholar]
11. Boenigk J, Arndt H. 2000. Particle handling during interception feeding by four species of heterotrophic nanoflagellates. J. Eukaryot. Microbiol. 47:350–58
    [Google Scholar]
12. Boenigk J, Arndt H. 2002. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie van Leeuwenhoek 81:465–80
    [Google Scholar]
13. Bruggeman J, Kooijman SALM. 2007. A biodiversity-inspired approach to aquatic ecosystem modeling. Limnol. Oceanogr. 52:1533–44
    [Google Scholar]
14. Bruno E, Borg CMA, Kiørboe T. 2012. Prey detection and prey capture in copepod nauplii. PLOS ONE 7:e47906
    [Google Scholar]
15. Burki F, Roger AJ, Brown MW, Simpson AGB. 2020. The new tree of eukaryotes. Trends Ecol. Evol. 35:43–55
    [Google Scholar]
16. Cachon M, Cachon J, Cosson J, Greuet C, Huitorel P. 1991. Dinoflagellate flagella adopt various conformations in response to different needs. Biol. Cell 71:175–82
    [Google Scholar]
17. Cadier M, Andersen KH, Visser AW, Kiørboe T. 2019. Competition–defense tradeoff increases the diversity of microbial plankton communities and dampens trophic cascades. Oikos 128:1027–40
    [Google Scholar]
18. Cavalier-Smith T. 2013. Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa. Eur. J. Protistol. 49:115–78
    [Google Scholar]
19. Chakraborty S, Nielsen LT, Andersen KH. 2017. Trophic strategies of unicellular plankton. Am. Nat. 189:E77–90
    [Google Scholar]
20. Chakraborty S, Pančić M, Andersen KH, Kiørboe T. 2019. The cost of toxin production in phytoplankton: the case of PST producing dinoflagellates. ISME J. 13:64–75
    [Google Scholar]
21. Christensen-Dalsgaard KK, Fenchel T. 2003. Increased filtration efficiency of attached compared to free-swimming flagellates. Aquat. Microb. Ecol. 33:77–86
    [Google Scholar]
22. Christensen-Dalsgaard KK, Fenchel T. 2004. Complex flagellar motions and swimming patterns of the flagellates Paraphysomonas vestita and Pteridomonas danica. Protist 155:79–87
    [Google Scholar]
23. Coles VJ, Stukel MR, Brooks MT, Burd A, Crump BC et al. 2017. Ocean biogeochemistry modeled with emergent trait-based genomics. Science 358:1149–54
    [Google Scholar]
24. Corno G, Jürgens K. 2006. Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Appl. Environ. Microbiol. 72:78–86
    [Google Scholar]
25. Dadon-Pilosof A, Conley KR, Jacobi Y, Haber M, Lombard F et al. 2017. Surface properties of SAR11 bacteria facilitate grazing avoidance. Nat. Microbiol. 2:1608–15
    [Google Scholar]
26. Dayel MJ, King N. 2014. Prey capture and phagocytosis in the choanoflagellate Salpingoeca rosetta. PLOS ONE 9:e95577
    [Google Scholar]
27. del Campo J, Balagué V, Forn I, Lekunberri I, Massana R. 2013a. Culturing bias in marine heterotrophic flagellates analyzed through seawater enrichment incubations. Microb. Ecol. 66:489–99
    [Google Scholar]
28. del Campo J, Not F, Forn I, Sieracki ME, Massana R. 2013b. Taming the smallest predators of the oceans. ISME J. 7:351–58
    [Google Scholar]
29. Dölger J, Kiørboe T, Andersen A. 2019. Dense dwarfs versus gelatinous giants: the trade-offs and physiological limits determining the body plan of planktonic filter feeders. Am. Nat. 194:E30–40
    [Google Scholar]
30. Dölger J, Nielsen LT, Kiørboe T, Andersen A. 2017. Swimming and feeding of mixotrophic biflagellates. Sci. Rep. 7:39892
    [Google Scholar]
31. Driscoll WW, Hackett JD, Ferrière R. 2016. Eco-evolutionary feedbacks between private and public goods: evidence from toxic algal blooms. Ecol. Lett. 19:81–97
    [Google Scholar]
32. Edwards KF, Klausmeier CA, Litchman E. 2011. Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton. Ecology 92:2085–95
    [Google Scholar]
33. Edwards KF, Litchman E, Klausmeier CA. 2013. Functional traits explain phytoplankton community structure and seasonal dynamics in a marine ecosystem. Ecol. Lett. 16:56–63
    [Google Scholar]
34. Fenchel T. 1982. Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol. Prog. Ser. 8:211–23
    [Google Scholar]
35. Fenchel T. 1986. Protozoan filter feeding. Prog. Protistol. 1:65–113
    [Google Scholar]
36. Fenchel T. 2001. How dinoflagellates swim. Protist 152:329–38
    [Google Scholar]
37. Fenchel T. 2019. Filter-feeding in colonial protists. Protist 170:283–86
    [Google Scholar]
38. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:427–51
    [Google Scholar]
39. Gawryluk RMR, Tikhonenkov DV, Hehenberger E, Husnik F, Mylnikov AP, Keeling PJ. 2019. Non-photosynthetic predators are sister to red algae. Nature 572:240–43
    [Google Scholar]
40. Granéli E, Turner JT. 2006. Ecology of Harmful Algae Berlin: Springer
41. Guillonneau R, Murphy ARJ, Teng Z-J, Wang P, Zhang Y-Z et al. 2022. Trade-offs of lipid remodeling in a marine predator-prey interaction in response to phosphorus limitation. PNAS 119:e2203057119
    [Google Scholar]
42. Hansen PJ, Bjørnsen PK, Hansen BW. 1997. Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol. Oceanogr. 42:687–704
    [Google Scholar]
43. Higdon JJL. 1979. A hydrodynamic analysis of flagellar propulsion. J. Fluid Mech. 90:685–711
    [Google Scholar]
44. Holwill MA, Sleigh M. 1967. Propulsion by hispid flagella. J. Exp. Biol. 47:267–76
    [Google Scholar]
45. Jabbarzadeh M, Fu HC. 2018. Viscous constraints on microorganism approach and interaction. J. Fluid Mech. 851:715–38
    [Google Scholar]
46. Jahn TL, Landman MD, Fonseca JR. 1964. The mechanism of locomotion of flagellates. II. Function of the mastigonemes of Ochromonas. J. Protozool. 3:291–96
    [Google Scholar]
47. Jakobsen HH. 2001. Escape response of planktonic protists to fluid mechanical signals. Mar. Ecol. Prog. Ser. 214:67–78
    [Google Scholar]
48. Jékely G, Arendt D. 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. BioEssays 28:191–98
    [Google Scholar]
49. Jiang H. 2011. Why does the jumping ciliate Mesodinium rubrum possess an equatorially located propulsive ciliary belt?. J. Plankton Res. 33:998–1011
    [Google Scholar]
50. Jiang H, Paffenhöfer G. 2008. Hydrodynamic signal perception by the copepod Oithona plumifera. Mar. Ecol. Prog. Ser. 373:37–52
    [Google Scholar]
51. Johansen J, Pinhassi J, Blackburn N, Zwefel U, Hagström Å. 2002. Variability in motility characteristics among marine bacteria. Aquat. Mar. Ecol. 28:229–37
    [Google Scholar]
52. Jonsson PR, Pavia H, Toth G. 2009. Formation of harmful algal blooms cannot be explained by allelopathic interactions. PNAS 106:11177–82
    [Google Scholar]
53. Jousset A. 2012. Ecological and evolutive implications of bacterial defences against predators. Environ. Microbiol. 14:1830–43
    [Google Scholar]
54. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ. 2008. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 6:162–68
    [Google Scholar]
55. Kamennaya NA, Kennaway G, Sleigh MA, Zubkov MV. 2022. Notable predominant morphology of the smallest most abundant protozoa of the open ocean revealed by electron microscopy. J. Plankton Res. 44:542–58
    [Google Scholar]
56. Kawachi M, Inouye I. 1995. Functional roles of the haptonema and the spine scales in the feeding process of Chrysochromulina spinifera (Fournier) Pienaar et Norris (Haptophyta = Prymnesiophyta). Phycologia 34:193–200
    [Google Scholar]
57. Kawachi M, Inouye I, Maeda O, Chihara M. 1991. The haptonema as a food-capturing device: observations on Chrysochromulina hirta (Prymnesiophyceae). Phycologia 30:563–73
    [Google Scholar]
58. Keeling PJ. 2013. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 64:583–607
    [Google Scholar]
59. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605–18
    [Google Scholar]
60. Kenitz KM, Visser AW, Mariani P, Andersen KH. 2017. Seasonal succession in zooplankton feeding traits reveals trophic trait coupling. Limnol. Oceanogr. 62:1184–97
    [Google Scholar]
61. Kiørboe T. 2008. A Mechanistic Approach to Plankton Ecology Princeton, NJ: Princeton Univ. Press
62. Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biol. Rev. Camb. Philos. Soc. 86:311–39
    [Google Scholar]
63. Kiørboe T, Andersen A, Langlois VJ, Jakobsen HH, Bohr T. 2009. Mechanisms and feasibility of prey capture in ambush-feeding zooplankton. PNAS 106:12394–99
    [Google Scholar]
64. Kiørboe T, Jiang H, Gonçalves RJ, Nielsen LT, Wadhwa N. 2014. Flow disturbances generated by feeding and swimming zooplankton. PNAS 111:11738–43
    [Google Scholar]
65. Kiørboe T, Visser A, Andersen KH. 2018. A trait-based approach to ocean ecology. ICES J. Mar. Sci. 75:1849–63
    [Google Scholar]
66. Kirkegaard JB, Goldstein RE. 2016. Filter-feeding, near-field flows, and the morphologies of colonial choanoflagellates. Phys. Rev. E. 94:052401
    [Google Scholar]
67. Klapper M, Arp J, Günther M, Stallforth P. 2018. The role of bacterial natural products in predator defense. Synlett 29:537–41
    [Google Scholar]
68. Koehl MAR. 2021. Selective factors in the evolution of multicellularity in choanoflagellates. J. Exp. Zool. B 336:315–26
    [Google Scholar]
69. Ku C, Roettger M, Zimorski V, Nelson-Sathi S, Sousa FL, Martin WF. 2014. Plastid origin: who, when and why?. Acta Soc. Bot. Pol. 83:281–89
    [Google Scholar]
70. Kumler WE, Jorge J, Kim PM, Iftekhar N, Koehl MAR 2020. Does formation of multicellular colonies by choanoflagellates affect their susceptibility to capture by passive protozoan predators?. J. Eukaryot. Microbiol. 67:555–65
    [Google Scholar]
71. Langlois V, Andersen A, Bohr T, Visser A, Kiørboe T. 2009. Significance of swimming and feeding currents for nutrient uptake in osmotrophic and interception feeding flagellates. Aquat. Microb. Ecol. 54:35–44
    [Google Scholar]
72. Lauga E. 2020. The Fluid Dynamics of Cell Motility Cambridge, UK: Cambridge Univ. Press
73. Leadbeater BSC, Yu Q, Kent J, Stekel DJ. 2009. Three-dimensional images of choanoflagellate loricae. Proc. R. Soc. B 276:3–11
    [Google Scholar]
74. L'Etoile NJ, King-Smith C. 2020. Rosette colonies of choanoflagellates (Salpingoeca rosetta) show increased food vacuole formation compared with single swimming cells. J. Eukaryot. Microbiol. 67:263–67
    [Google Scholar]
75. Li Q, Edwards KF, Schvarcz CR, Steward GF. 2022. Broad phylogenetic and functional diversity among mixotrophic consumers of Prochlorococcus. ISME J. 16:1557–69
    [Google Scholar]
76. Magar V, Pedley TJ. 2005. Average nutrient uptake by a self-propelled unsteady squirmer. J. Fluid Mech. 539:93
    [Google Scholar]
77. Matz C, Jürgens K. 2001. Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl. Environ. Microbiol. 67:814–20
    [Google Scholar]
78. Matz C, Jürgens K. 2005. High motility reduces grazing mortality of planktonic bacteria. Appl. Environ. Microbiol. 71:921–29
    [Google Scholar]
79. Matz C, Kjelleberg S. 2005. Off the hook – how bacteria survive protozoan grazing. Trends Microbiol. 13:302–7
    [Google Scholar]
80. Mazzola M, De Bruijn I, Cohen MF, Raaijmakers JM. 2009. Protozoan-induced regulation of cyclic lipopeptide biosynthesis is an effective predation defense mechanism for Pseudomonas fluorescens. Appl. Environ. Microbiol. 75:6804–11
    [Google Scholar]
81. Miyasaka I, Nanba K, Furuya K, Nimura Y, Azuma A. 2004. Functional roles of the transverse and longitudinal flagella in the swimming motility of Prorocentrum minimum (Dinophyceae). J. Exp. Biol. 207:3055–66
    [Google Scholar]
82. Moestrup Ø. 1982. Flagellar structure in algae: a review, with new observations particularly on the Chrysophyceae, Phaeophyceae (Fucophyceae), Euglenophyceae, and Reckertia. Phycologia 21:427–528
    [Google Scholar]
83. Moreira D, López-García P. 2014. The rise and fall of picobiliphytes: how assumed autotrophs turned out to be heterotrophs. BioEssays 36:468–74
    [Google Scholar]
84. Nguyen H, Ortiz R, Cortez R, Fauci L. 2011. The action of waving cylindrical rings in a viscous fluid. J. Fluid Mech. 671:574–86
    [Google Scholar]
85. Nielsen LT, Asadzadeh SS, Dölger J, Walther JH, Kiørboe T, Andersen A. 2017. Hydrodynamics of microbial filter feeding. PNAS 114:9373–78
    [Google Scholar]
86. Nielsen LT, Kiørboe T. 2015. Feeding currents facilitate a mixotrophic way of life. ISME J. 9:2117–27
    [Google Scholar]
87. Nielsen LT, Kiørboe T. 2021. Foraging trade-offs, flagellar arrangements, and flow architecture of planktonic protists. PNAS 118:e2009930118
    [Google Scholar]
88. Nielsen TG, Kiørboe T, Bjørnsen PK. 1990. Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar. Ecol. Prog. Ser. 62:21–35
    [Google Scholar]
89. Obiol A, Muhovic I, Massana R. 2021. Oceanic heterotrophic flagellates are dominated by a few widespread taxa. Limnol. Oceanogr. 66:4240–53
    [Google Scholar]
90. Parfrey LW, Lahr DJG, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. PNAS 108:13624–29
    [Google Scholar]
91. Park G, Dam HG. 2021. Cell-growth gene expression reveals a direct fitness cost of grazer-induced toxin production in red tide dinoflagellate prey. Proc. R. Soc. B 288:20202480
    [Google Scholar]
92. Peacock MB, Kudela RM. 2014. Evidence for active vertical migration by two dinoflagellates experiencing iron, nitrogen, and phosphorus limitation. Limnol. Oceanogr. 59:660–73
    [Google Scholar]
93. Pepper RE, Riley EE, Baron M, Hurot T, Nielsen LT et al. 2021. The effect of external flow on the feeding currents of sessile microorganisms. J. R. Soc. Interface 18:20200953
    [Google Scholar]
94. Pettitt ME. 2001. Prey capture and ingestion in choanoflagellates PhD Thesis Univ. Birmingham Birmingham, UK:
95. Pinskey JM, Lagisetty A, Gui L, Phan N, Reetz E et al. 2022. Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates. eLife 11:78133
    [Google Scholar]
96. Prowe AEF, Visser AW, Andersen KH, Chiba S, Kiørboe T. 2019. Biogeography of zooplankton feeding strategy. Limnol. Oceanogr. 64:661–78
    [Google Scholar]
97. Rengefors K, Kremp A, Reusch TBH, Wood AM. 2017. Genetic diversity and evolution in eukaryotic phytoplankton: revelations from population genetic studies. J. Plankton Res. 39:165–79
    [Google Scholar]
98. Roper M, Dayel MJ, Pepper RE, Koehl MAR 2013. Cooperatively generated stresslet flows supply fresh fluid to multicellular choanoflagellate colonies. Phys. Rev. Lett. 110:228104
    [Google Scholar]
99. Ryderheim F, Selander E, Kiørboe T. 2021. Predator-induced defence in a dinoflagellate generates benefits without direct costs. ISME J. 15:2107–16
    [Google Scholar]
100. Salcher MM, Pernthaler J, Psenner R, Posch T. 2005. Succession of bacterial grazing defense mechanisms against protistan predators in an experimental microbial community. Aquat. Microb. Ecol. 38:215–29
     [Google Scholar]
101. Schavemaker PE, Lynch M. 2022. Flagellar energy costs across the tree of life. eLife 11:77266
     [Google Scholar]
102. Schmitz OJ, Suttle KB. 2001. Effects of top predator species on direct and indirect interactions in a food web. Ecology 82:2072
     [Google Scholar]
103. Selander E, Thor P, Toth G, Pavia H. 2006. Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc. R. Soc. B 273:1673–80
     [Google Scholar]
104. Serra-Pompei C, Soudijn F, Visser AW, Kiørboe T, Andersen KH. 2020. A general size- and trait-based model of plankton communities. Prog. Oceanogr. 189:102473
     [Google Scholar]
105. Seymour JR, Marcos, Stocker R. 2009. Resource patch formation and exploitation throughout the marine microbial food web. Am. Nat. 173:E15–29
     [Google Scholar]
106. Simpson AGB, Patterson DJ. 1999. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the “excavate hypothesis. .” Eur. J. Protistol. 35:353–70
     [Google Scholar]
107. Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY. 2016. Fear of large carnivores causes a trophic cascade. Nat. Commun. 7:10698
     [Google Scholar]
108. Suzuki-Tellier S, Andersen A, Kiørboe T. 2022. Mechanisms and fluid dynamics of foraging in heterotrophic nanoflagellates. Limnol. Oceanogr. 67:1287–98
     [Google Scholar]
109. Thingstad TF. 2022. Competition-defense trade-offs in the microbial world. PNAS 119:e2213092119
     [Google Scholar]
110. Tikhonenkov DV. 2020. Predatory flagellates – the new recently discovered deep branches of the eukaryotic tree and their evolutionary and ecological significance. Protistology 14:15–22
     [Google Scholar]
111. Tikhonenkov DV, Mikhailov KV, Gawryluk RMR, Belyaev AO, Mathur V et al. 2022. Microbial predators form a new supergroup of eukaryotes. Nature 612:714–19
     [Google Scholar]
112. Tilman D. 1990. Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos 58:3–15
     [Google Scholar]
113. Tophøj J, Wollenberg RD, Sondergaard TE, Eriksen NT. 2018. Feeding and growth of the marine heterotrophic nanoflagellates, Procryptobia sorokini and Paraphysomonas imperforata on a bacterium, Pseudoalteromonas sp. with an inducible defence against grazing. PLOS ONE 13:e0195935
     [Google Scholar]
114. Unrein F, Gasol J, Not F, Forn I, Massane R. 2014. Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J. 8:164–76
     [Google Scholar]
115. Våge S, Bratbak G, Egge J, Heldal M, Larsen A et al. 2018. Simple models combining competition, defence and resource availability have broad implications in pelagic microbial food webs. Ecol. Lett. 21:1440–52
     [Google Scholar]
116. Våge S, Storesund JE, Giske J, Thingstad TF. 2014. Optimal defense strategies in an idealized microbial food web under trade-off between competition and defense. PLOS ONE 9:e101415
     [Google Scholar]
117. van Someren Gréve H, Kiørboe T, Almeda R 2019. Bottom-up behaviourally mediated trophic cascades in plankton food webs. Proc. R. Soc. B 286:20181664
     [Google Scholar]
118. Velho Rodrigues MF, Lisicki M, Lauga E. 2021. The bank of swimming organisms at the micron scale (BOSO-Micro). PLOS ONE 16:e0252291
     [Google Scholar]
119. Ward BA, Dutkiewicz S, Jahn O, Follows MJ. 2012. A size-structured food-web model for the global ocean. Limnol. Oceanogr. 57:1877–91
     [Google Scholar]
120. Wetherbee R, Andersen RA. 1992. Flagella of a chrysophycean alga play an active role in prey capture and selection: direct observations on Epipyxis pulchra using image enhanced video microscopy. Protoplasma 166:1–7
     [Google Scholar]
121. Xu J, Kiørboe T. 2018. Toxic dinoflagellates produce true grazer deterrents. Ecology 99:2240–49
     [Google Scholar]