Risk-reward trade-off during carbon starvation generates dichotomy in motility endurance among marine bacteria.

Journal: Nature microbiology
Published Date:

Abstract

Copiotrophic marine bacteria contribute to the control of carbon storage in the ocean by remineralizing organic matter. Motility presents copiotrophs with a risk-reward trade-off: it is highly beneficial in seeking out sparse nutrient hotspots, but energetically costly. Here we studied the motility endurance of 26 marine isolates, representing 18 species, using video microscopy and cell tracking over 2 days of carbon starvation. We found that the trade-off results in a dichotomy among marine bacteria, in which risk-averse copiotrophs ceased motility within hours ('limostatic'), whereas risk-prone copiotrophs converted ~9% of their biomass per day into energy to retain motility for the 2 days of observation ('limokinetic'). Using machine learning classifiers, we identified a genomic component associated with both strategies, sufficiently robust to predict the response of additional species with 86% accuracy. This dichotomy can help predict the prevalence of foraging strategies in marine microbes and inform models of ocean carbon cycles.

Authors

  • Johannes M Keegstra
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland. keegstra@ifu.baug.ethz.ch.
  • Zachary C Landry
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Sophie T Zweifel
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Benjamin R K Roller
    EAWAG - Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland.
  • Dieter A Baumgartner
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Francesco Carrara
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Clara Martínez-Pérez
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Estelle E Clerc
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland.
  • Martin Ackermann
    EAWAG - Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland.
  • Roman Stocker
    Institute for Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland. romanstocker@ethz.ch.