Abstract

Phytoplankton exist in genetically diverse populations, but are often studied as single lineages (single strains), so that interpreting single-lineage studies relies critically on understanding how microbial growth differs with social milieu, defined as the presence or absence of conspecifics. The properties of lineages grown alone often fail to predict the growth of these same lineages in the presence of conspecifics, and this discrepancy points towards an opportunity to improve our understanding of the factors that affect lineage growth rates. We demonstrate that different lineages of a marine picoplankter modulate their maximum lineage growth rate in response to the presence of non-self conspecifics, even when resource competition is effectively absent. This explains why growth rates of lineages in isolation do not reliably predict their growth rates in mixed culture, or the lineage composition of assemblages under conditions of rapid growth. The diversity of growth strategies observed here are consistent with lineage-specific energy allocation that depends on social milieu. Since lineage growth is only one of many traits determining fitness in natural assemblages, we hypothesize that intraspecific variation in growth strategies should be common, with more strategies possible in ameliorated environments that support higher maximum growth rates, such as high CO2 for many marine picoplankton.

Highlights

  • Microbial primary producers, composed mainly of phytoplankton, form the base of aquatic ecosystems and link organisms to their environment through their role in nutrient cycling [1,2]

  • Explanations of lineage frequencies in multi-lineage assemblages of phytoplankton are based on lineage growth rates being determined by differences in nutrient affinities, often modulated by temperature and light [8], but assume that these characters do not change in a given lineage growing in a given abiotic environment and cell density

  • We show that Ostrecococcus reacts to non-self conspecifics: maximum lineage growth rates in monoculture and mixed culture can, and often do, differ at the same resource levels and cell densities

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Summary

Introduction

Microbial primary producers, composed mainly of phytoplankton, form the base of aquatic ecosystems and link organisms to their environment through their role in nutrient cycling [1,2]. Explanations of lineage frequencies in multi-lineage assemblages of phytoplankton are based on lineage growth rates being determined by differences in nutrient affinities, often modulated by temperature and light [8], but assume that these characters do not change in a given lineage growing in a given abiotic environment and cell density Under this set of assumptions, lineages interact only through their effects on resources and cell density, but phytoplankton lineages do not respond to the presence of non-self conspecifics directly. We posit that lineages in low-density, resource-replete environments can modulate their growth strategies in response to social milieu, and that this could explain why lineage growth rates in monoculture sometimes fail to predict lineage frequencies in mixed culture in the absence of competition Such environments are common in laboratory batch cultures, where much of our data on phytoplankton growth is gathered, as well as at the beginning of algal blooms, when cell densities are low and nutrient levels are relatively high. Maximum lineage growth rate varies within species [11,12,13,14,15], but how lineages modulate growth strategies with social milieu is rarely studied, despite being vital for scaling up from single to multi-lineage populations

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