Title: Basin-scale biogeography of marine phytoplankton reflects cellular-scale optimization of metabolism and physiology

Journal Article · · Science Advances
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [3]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [8]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Univ. of Hawaii at Manoa, Honolulu, HI (United States)
  2. Oregon State Univ., Corvallis, OR (United States)
  3. Chalmers University of Technology, Gothenburg (Sweden)
  4. Dalhousie Univ., Halifax, NS (Canada)
  5. Mount Allison, Sackville, NB (Canada)
  6. Flatiron Institute, New York, NY (United States)
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  8. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Extensive microdiversity within Prochlorococcus, the most abundant marine cyanobacterium, occurs at scales from a single droplet of seawater to ocean basins. To interpret the structuring role of variations in genetic potential, as well as metabolic and physiological acclimation, we developed a mechanistic constraint-based modeling framework that incorporates the full suite of genes, proteins, metabolic reactions, pigments, and biochemical compositions of 69 sequenced isolates spanning the Prochlorococcus pangenome. Optimizing each strain to the local, observed physical and chemical environment along an Atlantic Ocean transect, we predicted variations in strain-specific patterns of growth rate, metabolic configuration, and physiological state, defining subtle niche subspaces directly attributable to differences in their encoded metabolic potential. Predicted growth rates covaried with observed ecotype abundances, affirming their significance as a measure of fitness and inferring a nonlinear density dependence of mortality. Our study demonstrates the potential to interpret global-scale ecosystem organization in terms of cellular-scale processes.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
Simons Foundation; USDOE Office of Science (SC)
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1841873
Report Number(s):
PNNL-SA-169821
Journal Information:
Science Advances, Journal Name: Science Advances Journal Issue: 3 Vol. 8; ISSN 2375-2548
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
English

References (86)

Data from: Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus dataset January 2015
Prediction of diffusion coefficients for nonelectrolytes in dilute aqueous solutions journal May 1974
An improved protocol for flow cytometry analysis of phytoplankton cultures and natural samples: An Improved Protocol for Flow Cytometry Analysis journal August 2014
Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the S outh E ast P acific O cean journal January 2016
Niche partitioning of low‐light adapted Prochlorococcus subecotypes across oceanographic gradients of the North Pacific Subtropical Front journal January 2021
Comparing Prochlorococcus temperature niches in the lab and across ocean basins journal May 2021
Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies journal March 2002
Basin-scale variability of phytoplankton biomass, production and growth in the Atlantic Ocean journal May 2000
Carbohydrate analysis by a phenol–sulfuric acid method in microplate format journal April 2005
Roles of xanthophyll carotenoids in protection against photoinhibition and oxidative stress in the cyanobacterium Synechococcus sp. strain PCC 7002 journal December 2010
Prochlorococcus journal June 2017
Comparative genomics: the bacterial pan-genome journal October 2008
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis journal May 2009
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry journal December 2009
Machine Learning Applied to Predicting Microorganism Growth Temperatures and Enzyme Catalytic Optima journal May 2019
Studies in Diffusion. ii. a Kinetic Theory of Diffusion in Liquid Systems journal October 1930
Natural variability of phytoplanktonic absorption in oceanic waters: Influence of the size structure of algal populations journal January 2004
Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum journal January 2007
Particulate organic matter flux and planktonic new production in the deep ocean journal December 1979
Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule journal July 2007
Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans journal May 2010
Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity journal March 2009
Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter journal March 2013
Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres journal June 2008
A protocol for generating a high-quality genome-scale metabolic reconstruction journal January 2010
Template-based protein structure modeling using the RaptorX web server journal July 2012
In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp. using genome-scale modelling journal December 2010
MEMOTE for standardized genome-scale metabolic model testing journal March 2020
Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0 journal February 2019
A synthesis of bacterial and archaeal phenotypic trait data journal June 2020
Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus journal September 2014
Single cell genomes of Prochlorococcus, Synechococcus, and sympatric microbes from diverse marine environments journal September 2018
Salmonella modulates metabolism during growth under conditions that induce expression of virulence genes journal January 2013
Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis journal January 2012
Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus journal May 2013
Impact of ocean phytoplankton diversity on phosphate uptake journal November 2014
The bioenergetic costs of a gene journal November 2015
Metabolic evolution and the self-organization of ecosystems journal March 2017
Minimal cobalt metabolism in the marine cyanobacterium Prochlorococcus journal June 2020
Trophic interactions with heterotrophic bacteria limit the range of Prochlorococcus journal January 2022
The Light: Nutrient Ratio in Lakes: The Balance of Energy and Materials Affects Ecosystem Structure and Process journal December 1997
eQuilibrator--the biochemical thermodynamics calculator journal November 2011
Photoacclimation of Prochlorococcus sp. (Prochlorophyta) Strains Isolated from the North Atlantic and the Mediterranean Sea journal January 1993
The Metabolic Network of Synechocystis sp. PCC 6803: Systemic Properties of Autotrophic Growth journal July 2010
Physiological role and regulation of glutamate dehydrogenase in Prochlorococcus sp. strain MIT9313 journal February 2009
Niche Partitioning Among Prochlorococcus Ecotypes Along Ocean-Scale Environmental Gradients journal March 2006
Emergent Biogeography of Microbial Communities in a Model Ocean journal March 2007
The Tricarboxylic Acid Cycle in Cyanobacteria journal December 2011
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus journal April 2014
Growth of Prochlorococcus, a Photosynthetic Prokaryote, in the Equatorial Pacific Ocean journal June 1995
Prochlorococcus Ecotype Abundances in the North Atlantic Ocean As Revealed by an Improved Quantitative PCR Method journal January 2006
Genome-Wide Analysis of Light Sensing in Prochlorococcus journal September 2006
The Presence of Glutamate Dehydrogenase Is a Selective Advantage for the Cyanobacterium Synechocystis sp. Strain PCC 6803 under Nonexponential Growth Conditions journal February 1999
Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance journal March 1999
Model for bacterial culture growth rate throughout the entire biokinetic temperature range. journal January 1983
Quantitative Proteomics Shows Extensive Remodeling Induced by Nitrogen Limitation in Prochlorococcus marinus SS120 journal May 2017
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses journal May 2016
Prochlorococcus : Advantages and Limits of Minimalism journal January 2010
Computationally efficient flux variability analysis journal September 2010
In silico approaches to study mass and energy flows in microbial consortia: a syntrophic case study journal January 2009
DFBAlab: a fast and reliable MATLAB code for dynamic flux balance analysis journal December 2014
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities journal February 2012
RAVEN 2.0: A versatile toolbox for metabolic network reconstruction and a case study on Streptomyces coelicolor journal October 2018
A steady-state model of microbial acclimation to substrate limitation journal August 2020
Light Variability Illuminates Niche-Partitioning among Marine Picocyanobacteria journal December 2007
Context-Specific Metabolic Model Extraction Based on Regularized Least Squares Optimization journal July 2015
Ecological Stoichiometry book December 2003
Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean journal January 1997
Dynamic Allocation of Carbon Storage and Nutrient-Dependent Exudation in a Revised Genome-Scale Model of Prochlorococcus journal February 2021
Differential Activity of Coexisting Prochlorococcus Ecotypes journal November 2019
Prochlorococcus and Synechococcus have Evolved Different Adaptive Mechanisms to Cope with Light and UV Stress journal January 2012
Metabolic Network Modeling of Microbial Interactions in Natural and Engineered Environmental Systems journal May 2016
The Macromolecular Basis of Phytoplankton C:N:P Under Nitrogen Starvation journal April 2019
Scratching Beneath the Surface: A Model to Predict the Vertical Distribution of Prochlorococcus Using Remote Sensing journal May 2018
A transportable microprocessor-controlled precise Winkler titration suitable for field station and shipboard use1 journal May 1982
Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting journal January 1994
Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates journal May 1999
Diel variations in Prochlorococcus optical properties journal November 2002
Elemental composition of marine Prochlorococcus and Synechococcus : Implications for the ecological stoichiometry of the sea journal September 2003
Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis journal September 2003
Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean journal September 2007
Culturing the marine cyanobacterium Prochlorococcus: Prochlorococcus culturing journal October 2007
Photosynthesis–irradiance parameters of marine phytoplankton: synthesis of a global data set journal January 2018
PanGEM Toolbox - Prochlorococcus pangenome dataset January 2021
RAVEN 2.0: a versatile toolbox for metabolic network reconstruction and a case study on Streptomyces coelicolor dataset January 2018
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome journal January 2018