Oceans host communities of plankton composed of relatively few abundant species and many rare species. The number of rare protist species in these communities, as estimated in metagenomic studies, decays as a steep power law of their abundance. The ecological factors at the origin of this pattern remain elusive. We propose that chaotic advection by oceanic currents affects biodiversity patterns of rare species. To test this hypothesis, we introduce a spatially explicit coalescence model that reconstructs the species diversity of a sample of water. Our model predicts, in the presence of chaotic advection, a steeper power law decay of the species abundance distribution and a steeper increase of the number of observed species with sample size. A comparison of metagenomic studies of planktonic protist communities in oceans and in lakes quantitatively confirms our prediction. Our results support that oceanic currents positively affect the diversity of rare aquatic microbes.

Faculty of Tropical AgriSciences Czech University of Life Sciences Kamýcká 129 CZ 165 00 Prague Czech Republic

Okinawa Institute of Science and Technology Graduate University Onna Okinawa 904 0495 Japan

See more in PubMed

Finlay B. J., Global dispersal of free-living microbial eukaryote species. Science 296, 1061–1063 (2002). PubMed

L. G. M. Baas Becking, Geobiologie of Inleiding Tot De Milieukunde (WP Van Stockum & Zoon, 1934), pp. 18–19.

Fuhrman J. A., Microbial community structure and its functional implications. Nature 459, 193–199 (2009). PubMed

Stomp M., Huisman J., Mittelbach G. G., Litchman E., Klausmeier C. A., Large-scale biodiversity patterns in freshwater phytoplankton. Ecology 92, 2096–2107 (2011). PubMed

Sunagawa S., Coelho L. P., Chaffron S., Kultima J. R., Labadie K., Salazar G., Djahanschiri B., Zeller G., Mende D. R., Alberti A., Cornejo-Castillo F. M., Costea P. I., Cruaud C., d’Ovidio F., Engelen S., Ferrera I., Gasol J. M., Guidi L., Hildebrand F., Kokoszka F., Lepoivre C., Lima-Mendez G., Poulain J., Poulos B. T., Royo-Llonch M., Sarmento H., Vieira-Silva S., Dimier C., Picheral M., Searson S., Kandels-Lewis S.; Tara Oceans coordinators, Bowler C., de Vargas C., Gorsky G., Grimsley N., Hingamp P., Iudicone D., Jaillon O., Not F., Ogata H., Pesant S., Speich S., Stemmann L., Sullivan M. B., Weissenbach J., Wincker P., Karsenti E., Raes J., Acinas S. G., Bork P., Structure and function of the global ocean microbiome. Science 348, 1261359 (2015). PubMed

de Vargas C., Audic S., Henry N., Decelle J., Mahé F., Logares R., Lara E., Berney C., Le Bescot N., Probert I., Carmichael M., Poulain J., Romac S., Colin S., Aury J.-M., Bittner L., Chaffron S., Dunthorn M., Engelen S., Flegontova O., Guidi L., Horák A., Jaillon O., Lima-Mendez G., Lukeš J., Malviya S., Morard R., Mulot M., Scalco E., Siano R., Vincent F., Zingone A., Dimier C., Picheral M., Searson S., Kandels-Lewis S., Coordinators T. O., Acinas S. G., Bork P., Bowler C., Gorsky G., Grimsley N., Hingamp P., Iudicone D., Not F., Ogata H., Pesant S., Raes J., Sieracki M. E., Speich S., Stemmann L., Sunagawa S., Weissenbach J., Wincker P., Karsenti E., Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015). PubMed

Levin S. A., Community equilibria and stability, and an extension of the competitive exclusion principle. Am. Nat. 104, 413–423 (1970).

Hutchinson G. E., The paradox of the plankton. Am. Nat. 95, 137–145 (1961).

Scheffer M., Rinaldi S., Huisman J., Weissing F. J., Why plankton communities have no equilibrium: Solutions to the paradox. Hydrobiologia 491, 9–18 (2003).

Litchman E., Klausmeier C. A., Schofield O. M., Falkowski P. G., The role of functional traits and trade-offs in structuring phytoplankton communities: Scaling from cellular to ecosystem level. Ecol. Lett. 10, 1170–1181 (2007). PubMed

Litchman E., Klausmeier C. A., Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39, 615–639 (2008).

Bonachela J. A., Raghib M., Levin S. A., Dynamic model of flexible phytoplankton nutrient uptake. Proc. Natl. Acad. Sci. U.S.A. 108, 20633–20638 (2011). PubMed PMC

Kremer C. T., Klausmeier C. A., Coexistence in a variable environment: Eco-evolutionary perspectives. J. Theor. Biol. 339, 14–25 (2013). PubMed

Bonachela J. A., Klausmeier C. A., Edwards K. F., Litchman E., Levin S. A., The role of phytoplankton diversity in the emergent oceanic stoichiometry. J. Plankton Res. 38, 1021–1035 (2015).

Bracco A., Provenzale A., Scheuring I., Mesoscale vortices and the paradox of the plankton. Proc. Biol. Sci. 267, 1795–1800 (2000). PubMed PMC

Károlyi G., Péntek Á., Scheuring I., Tél T., Toroczkai Z., Chaotic flow: The physics of species coexistence. Proc. Natl. Acad. Sci. U.S.A. 97, 13661–13665 (2000). PubMed PMC

d’Ovidio F., De Monte S., Alvain S., Dandonneau Y., Lévy M., Fluid dynamical niches of phytoplankton types. Proc. Natl. Acad. Sci. U.S.A. 107, 18366–18370 (2010). PubMed PMC

McGillicuddy D. J., Jr., Mechanisms of physical-biological-biogeochemical interaction at the oceanic mesoscale. Ann. Rev. Mar. Sci. 8, 125–159 (2016). PubMed

Martiny J. B. H., Bohannan B. J. M., Brown J. H., Colwell R. K., Fuhrman J. A., Green J. L., Horner-Devine M. C., Kane M., Krumins J. A., Kuske C. R., Morin P. J., Naeem S., Ovreås L., Reysenbach A.-L., Smith V. H., Staley J. T., Microbial biogeography: Putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006). PubMed

Urban M. C., Leibold M. A., Amarasekare P., De Meester L., Gomulkiewicz R., Hochberg M. E., Klausmeier C. A., Loeuille N., De Mazancourt C., Norberg J., Pantel J. H., Strauss S. Y., Vellend M., Wade M. J., The evolutionary ecology of metacommunities. Trends Ecol. Evol. 23, 311–317 (2008). PubMed

Galand P. E., Casamayor E. O., Kirchman D. L., Lovejoy C., Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl. Acad. Sci. U.S.A. 106, 22427–22432 (2009). PubMed PMC

Chust G., Irigoien X., Chave J., Harris R. P., Latitudinal phytoplankton distribution and the neutral theory of biodiversity. Glob. Ecol. Biogeogr. 22, 531–543 (2013).

Wilkins D., van Sebille E., Rintoul S. R., Lauro F. M., Cavicchioli R., Advection shapes southern ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 4, 2457 (2013). PubMed

Sogin M. L., Morrison H. G., Huber J. A., Welch D. M., Huse S. M., Neal P. R., Arrieta J. M., Herndl G. J., Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl. Acad. Sci. U.S.A. 103, 12115–12120 (2006). PubMed PMC

Pedrós-Alió C., The rare bacterial biosphere. Ann. Rev. Mar. Sci. 4, 449–466 (2012). PubMed

Lynch M. D. J., Neufeld J. D., Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229 (2015). PubMed

Magurran A. E., Henderson P. A., Explaining the excess of rare species in natural species abundance distributions. Nature 422, 714–716 (2003). PubMed

Ulrich W., Ollik M., Frequent and occasional species and the shape of relative-abundance distributions. Divers. Distrib. 10, 263–269 (2004).

Ser-Giacomi E., Zinger L., Malviya S., De Vargas C., Karsenti E., Bowler C., De Monte S., Ubiquitous abundance distribution of non-dominant plankton across the global ocean. Nat. Ecol. Evol. 2, 1243–1249 (2018). PubMed

Jeraldo P., Sipos M., Chia N., Brulc J. M., Dhillon A. S., Konkel M. E., Larson C. L., Nelson K. E., Qu A., Schook L. B., Yang F., White B. A., Goldenfeld N., Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc. Natl. Acad. Sci. U.S.A. 109, 9692–9698 (2012). PubMed PMC

S. P. Hubbell, The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32) (Princeton Univ. Press, 2001).

Pigolotti S., Flammini A., Maritan A., Stochastic model for the species abundance problem in an ecological community. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 70, 011916 (2004). PubMed

He F., Deriving a neutral model of species abundance from fundamental mechanisms of population dynamics. Funct. Ecol. 19, 187–193 (2005).

Azaele S., Pigolotti S., Banavar J. R., Maritan A., Dynamical evolution of ecosystems. Nature 444, 926–928 (2006). PubMed

Lévy M., Franks P. J. S., Smith K. S., The role of submesoscale currents in structuring marine ecosystems. Nat. Commun. 9, 4758 (2018). PubMed PMC

Wares J. P., Pringle J. M., Drift by drift: Effective population size is limited by advection. BMC Evol. Biol. 8, 235 (2008). PubMed PMC

Herrerías-Azcué F., Pérez-Muñuzuri V., Galla T., Stirring does not make populations well mixed. Sci. Rep. 8, 4068 (2018). PubMed PMC

Pigolotti S., Benzi R., Jensen M. H., Nelson D. R., Population genetics in compressible flows. Phys. Rev. Lett. 108, 128102 (2012). PubMed

Plummer A., Benzi R., Nelson D. R., Toschi F., Fixation probabilities in weakly compressible fluid flows. Proc. Natl. Acad. Sci. U.S.A. 116, 373–378 (2019). PubMed PMC

Boenigk J., Wodniok S., Bock C., Beisser D., Hempel C., Grossmann L., Lange A., Jensen M., Geographic distance and mountain ranges structure freshwater protist communities on a European scale. Metabarcod. Metagenom. 2, e21519 (2018).

Pigolotti S., Benzi R., Perlekar P., Jensen M. H., Toschi F., Nelson D. R., Growth, competition and cooperation in spatial population genetics. Theor. Popul. Biol. 84, 72–86 (2013). PubMed

Rosindell J., Wong Y., Etienne R. S., A coalescence approach to spatial neutral ecology. Eco. Inform. 3, 259–271 (2008).

Pigolotti S., Cencini M., Molina D., Muñoz M. A., Stochastic spatial models in ecology: A statistical physics approach. J. Stat. Phys. 172, 44–73 (2018).

Bower A. S., A simple kinematic mechanism for mixing fluid parcels across a meandering jet. J. Phys. Oceanogr. 21, 173–180 (1991).

Cencini M., Lacorata G., Vulpiani A., Zambianchi E., Mixing in a meandering jet: A Markovian approximation. J. Phys. Oceanogr. 29, 2578–2594 (1999).

Martin A. P., Phytoplankton patchiness: The role of lateral stirring and mixing. Prog. Oceanogr. 57, 125–174 (2003).

Boffetta G., Lacorata G., Redaelli G., Vulpiani A., Detecting barriers to transport: A review of different techniques. Physica D 159, 58–70 (2001).

Pernice M. C., Giner C. R., Logares R., Perera-Bel J., Acinas S. G., Duarte C. M., Gasol J. M., Massana R., Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J. 10, 945–958 (2016). PubMed PMC

Filker S., Sommaruga R., Vila I., Stoeck T., Microbial eukaryote plankton communities of high-mountain lakes from three continents exhibit strong biogeographic patterns. Mol. Ecol. 25, 2286–2301 (2016). PubMed PMC

Crane H., The ubiquitous ewens sampling formula. Statist. Sci. 31, 1–19 (2016).

Morlon H., Schwilk D. W., Bryant J. A., Marquet P. A., Rebelo A. G., Tauss C., Bohannan B. J. M., Green J. L., Spatial patterns of phylogenetic diversity. Ecol. Lett. 14, 141–149 (2011). PubMed PMC

Villarino E., Watson J. R., Jönsson B., Gasol J. M., Salazar G., Acinas S. G., Estrada M., Massana R., Logares R., Giner C. R., Pernice M. C., Olivar M. P., Citores L., Corell J., Rodríguez-Ezpeleta N., Acuña J. L., Molina-Ramírez A., González-Gordillo J. I., Cózar A., Martí E., Cuesta J. A., Agustí S., Fraile-Nuez E., Duarte C. M., Irigoien X., Chust G., Large-scale ocean connectivity and planktonic body size. Nat. Commun. 9, 142 (2018). PubMed PMC

Marquet P. A., Espinoza G., Abades S. R., Ganz A., Rebolledo R., On the proportional abundance of species: Integrating population genetics and community ecology. Sci. Rep. 7, 16815 (2017). PubMed PMC

Milligan A. J., Oceanography: Plankton in an acidified ocean. Nat. Clim. Change 2, 489 (2012).

Kontoyiannis H., Watts D. R., Observations on the variability of the gulf stream path between 74°W and 70°W. J. Phys. Oceanogr. 24, 1999–2013 (1994).

Edgar R. C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010). PubMed

Rognes T., Flouri T., Nichols B., Quince C., Mahé F., VSEARCH: A versatile open source tool for metagenomics. PeerJ 4, e2584 (2016). PubMed PMC

Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011). PubMed PMC

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., Fierer N., Peña A. G., Goodrich J. K., Gordon J. I., Huttley G. A., Kelley S. T., Knights D., Koenig J. E., Ley R. E., Lozupone C. A., Mcdonald D., Muegge B. D., Pirrung M., Reeder J., Sevinsky J. R., Turnbaugh P. J., Walters W. A., Widmann J., Yatsunenko T., Zaneveld J., Knight R., Correspondence QIIME allows analysis of high-throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat. Methods. 7, 335–336 (2011). PubMed PMC

Martin M., Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10 (2011).

Bengtsson-Palme J., Ryberg M., Hartmann M., Branco S., Wang Z., Godhe A., De Wit P., Sánchez-García M., Ebersberger I., de Sousa F., Amend A. S., Jumpponen A., Unterseher M., Kristiansson E., Abarenkov K., Bertrand Y. J. K., Sanli K., Eriksson K. M., Vik U., Veldre V., Nilsson R. H., Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).

Richardson L. F., Atmospheric diffusion shown on a distance-neighbour graph. Proc. R. Soc. Lond. 110, 709–737 (1926).

Berti S., Santos F. A. D., Lacorata G., Vulpiani A., Lagrangian drifter dispersion in the southwestern atlantic ocean. J. Phys. Oceanogr. 41, 1659–1672 (2011).

Lacorata G., Aurell E., Vulpiani A., Drifter dispersion in the adriatic sea: Lagrangian data and chaotic model. Ann. Geophys. 19, 121–129 (2001).

T. Bohr, M. H. Jensen, G. Paladin, A. Vulpiani, Dynamical Systems Approach to Turbulence (Cambridge Univ. Press, 2005).