Picophytoplankton Niche Partitioning in the Warmest Oligotrophic Sea

Alexandra Coello-Camba,Susana Agustí

doi:10.3389/fmars.2021.651877

Alexandra Coello-Camba, Susana Agustí

Open Access

https://doi.org/10.3389/fmars.2021.651877

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Abstract

Pico-sizedSynechococcus,Prochlorococcus, and eukaryotes are the dominant photosynthetic organisms in the vast warm and oligotrophic regions of the ocean. In this paper, we aim to characterize the realized niches of the picophytoplanktonic community inhabiting the Red Sea, the warmest oligotrophic sea, which is considered to be a model for the future ocean. We quantify population abundances and environmental variables over several oceanographic surveys, and use stepwise regression, principal-component analysis (PCA), and compositional-data analysis to identify the realized niches of the three picophytoplanktonic groups. Water temperature varied from 21.4 to 32.4°C within the upper 200-m water column, with the warmest waters being found in the South, where nutrients increased.Synechococcusdominated the biomass, contributing 47.6% to the total picophytoplankton biomass, followed by picoeukaryotes (26.4%) andProchlorococcus(25.9%), whose proportions contrast significantly with those reported in the subtropical ocean, whereProchlorococcusprevails. There were positive and significant relationships between temperature and the three populations, although these were weak forProchlorococcus(R2= 0.08) and stronger and steeper forSynechococcus(R2= 0.57). The three populations centered their maximum abundances (Lorentzian fits) at similar low nutrient values.Synechococcuswere centered close to the surface at ≈77% of surface photosynthetically active radiation (PAR) and ≈30.6°C. The picoeukaryotes were centered at lower light (≈6.4% surface PAR) and warm waters (≈30°C).Prochlorococcuswas segregated from the surface waters and centered deep at low light (≈3.2% surface PAR). Light and temperature were the most influential factors determining the community composition, withSynechococcusdominating ∼74% of the picophytoplankton biovolume in the warmest (&gt;30°C) waters. In the warm and mesotrophic southern Red Sea, the moderate abundances of picoeukaryotes andSynechococcussuggest increasing competition with nano and microphytoplankton. Our observations agree with predictions of increasing vertical segregation of picophytoplankton communities with future warming and revealSynechococcus’s significant capacity to adapt to warming.

Highlights

Picophytoplankton comprises the smallest phytoplanktonic group (0.2–2 μm in size) and includes the populations of oceanic Prochlorococcus and Synechococcus picocyanobacteria, as well as a group of picoeukaryotes (Stockner, 1988; Raven, 1998; Partensky et al, 1999)
The chlorophyll a (Chl a) concentration, representing the total phytoplankton biomass, was low, averaging 0.28 (S.E. = ±0.02) μg L−1, and remaining below 1 μg L−1 except in two samples collected at deep chlorophyll maximum (DCM) depths in October, where the Chl a concentration reached 1.16 μg L−1 (Figure 2C)
The results indicated that, in the warmest waters (>30◦C), Synechococcus populations dominated the picophytoplankton community with an average biovolume proportion of 73.6%, while the average proportion of Prochlorococcus and picoeukaryotes decreased to 7.5 and 18.8%, respectively

Summary

Introduction

Picophytoplankton comprises the smallest phytoplanktonic group (0.2–2 μm in size) and includes the populations of oceanic Prochlorococcus and Synechococcus picocyanobacteria, as well as a group of picoeukaryotes (Stockner, 1988; Raven, 1998; Partensky et al, 1999). The genetic, molecular and physiological differences between organisms determine their fundamental niches, defined as the range of environmental conditions under which they are technically capable of living (Hutchinson, 1957). For Synechococcus, Prochlorococcus, and some picoeukaryotes, there is genetic and physiological evidence to outline their fundamental niches, as indicated by strong differences in their nutrient requirements (Moore et al, 2002; Bertilsson et al, 2003; Heldal et al, 2003; Zubkov et al, 2003), tolerance to light and ultraviolet radiation (Moore et al, 1995; Llabrés and Agustí, 2006), and thermal performances (Moore et al, 1995; Agawin et al, 1998; Chen et al, 2014). Other studies analyzed the niche partitioning of the three picophytoplankton populations (i.e., Synechococcus, Prochlorococcus, and picoeukaryotes) in both oceans and lakes (Winder, 2009; Bouman et al, 2011; Flombaum et al, 2020). Light, nutrients, and water-column mixing have been identified as significant influences upon picophytoplankton niche partitioning (Ferris and Palenik, 1998; Agustí, 2004; Bouman et al, 2011; Pittera et al, 2014)

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