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      Vertical migration by bulk phytoplankton sustains biodiversity and nutrient input to the surface ocean

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          Abstract

          Phytoplankton subsumes the great variety of unicellular photoautotrophs that perform roughly half of Earth’s primary production. They achieve this despite their challenging oceanic habitat, with opposing vertical gradients of nutrients (which often limit their growth near the surface) and light (which becomes limiting with increasing depth). Most phytoplankton species are commonly assumed to be incapable of moving actively between the zones of light and nutrient availability, which are separated vertically by from 30–120 m. Here we propose that a considerable fraction of phytoplankton vertically traverse these gradients over time scales from hours to weeks, employing variations of a common migration strategy to acquire multiple resources. We present a mechanistic Lagrangian model resolving phytoplankton growth linked to optimal migration behaviour and demonstrate unprecedented agreement of its calculated vertical CHL-a distributions with 773 profiles observed at five prominent marine time-series stations. Our simulations reveal that vertically cycling phytoplankton can pump up enough nutrient to sustain as much as half of oceanic Net Primary Production (NPP). Active locomotion is therefore a plausible mechanism enabling relatively high NPP in the oligotrophic surface ocean. Our simulations also predict similar fitness for a variety of very different migration strategies, which helps to explain the puzzling diversity of phytoplankton observed in the ocean.

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          Subsurface Chlorophyll Maximum Layers: Enduring Enigma or Mystery Solved?

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            Cyanobacterial dominance: The role of buoyancy regulation in dynamic lake environments

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              Evolution of phototaxis

              Phototaxis in the broadest sense means positive or negative displacement along a light gradient or vector. Prokaryotes most often use a biased random walk strategy, employing type I sensory rhodopsin photoreceptors and two-component signalling to regulate flagellar reversal. This strategy only allows phototaxis along steep light gradients, as found in microbial mats or sediments. Some filamentous cyanobacteria evolved the ability to steer towards a light vector. Even these cyanobacteria, however, can only navigate in two dimensions, gliding on a surface. In contrast, eukaryotes evolved the capacity to follow a light vector in three dimensions in open water. This strategy requires a polarized organism with a stable form, helical swimming with cilia and a shading or focusing body adjacent to a light sensor to allow for discrimination of light direction. Such arrangement and the ability of three-dimensional phototactic navigation evolved at least eight times independently in eukaryotes. The origin of three-dimensional phototaxis often followed a transition from a benthic to a pelagic lifestyle and the acquisition of chloroplasts either via primary or secondary endosymbiosis. Based on our understanding of the mechanism of phototaxis in single-celled eukaryotes and animal larvae, it is possible to define a series of elementary evolutionary steps, each of potential selective advantage, which can lead to pelagic phototactic navigation. We can conclude that it is relatively easy to evolve phototaxis once cell polarity, ciliary swimming and a stable cell shape are present.
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                Author and article information

                Contributors
                kai.wirtz@hzg.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                24 January 2020
                24 January 2020
                2020
                : 10
                : 1142
                Affiliations
                [1 ]Institute of Coastal Research, Helmholtz Centre Geesthacht, Geesthacht, Germany
                [2 ]ISNI 0000 0001 2191 0132, GRID grid.410588.0, Earth SURFACE System Research Center, Research Institute for Global Change, , JAMSTEC, ; Yokosuka, Japan
                Article
                57890
                10.1038/s41598-020-57890-2
                6981162
                31980670
                443a2ab6-dff4-41fd-bf59-972b9a5d07e5
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 2 August 2019
                : 8 January 2020
                Categories
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                © The Author(s) 2020

                Uncategorized
                behavioural ecology,biodiversity,biogeochemistry,biooceanography,community ecology,ecological modelling,marine biology

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