SAR11 Cells Rely on Enzyme Multifunctionality To Metabolize a Range of Polyamine Compounds.

Stephen E Noell,Jason R Graff,Christopher Suffridge,Kevin P Gable,Brian J Verwey,Gregory E Barrell,Stephen J Giovannoni,Jeff Morré,Ferdi L Hellweger,Nicole Dubilier

doi:10.1128/mbio.01091-21

Stephen E Noell, Jason R Graff + Show 8 more

Open Access

https://doi.org/10.1128/mbio.01091-21

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Journal: mBio	Publication Date: Aug 31, 2021
Citations: 11	License type: CC BY 4.0

Affiliation: Oregon State University, Technische Universität Berlin

Abstract

ABSTRACTIn the ocean surface layer and cell culture, the polyamine transport protein PotD of SAR11 bacteria is often one of the most abundant proteins detected. Polyamines are organic cations at seawater pH produced by all living organisms and are thought to be an important component of dissolved organic matter (DOM) produced in planktonic ecosystems. We hypothesized that SAR11 cells uptake and metabolize multiple polyamines and use them as sources of carbon and nitrogen. Metabolic footprinting and fingerprinting were used to measure the uptake of five polyamine compounds (putrescine, cadaverine, agmatine, norspermidine, and spermidine) in two SAR11 strains that represent the majority of SAR11 cells in the surface ocean environment, “Candidatus Pelagibacter” strain HTCC7211 and “Candidatus Pelagibacter ubique” strain HTCC1062. Both strains took up all five polyamines and concentrated them to micromolar or millimolar intracellular concentrations. Both strains could use most of the polyamines to meet their nitrogen requirements, but polyamines did not fully substitute for their requirements of glycine (or related compounds) or pyruvate (or related compounds). Our data suggest that potABCD transports all five polyamines and that spermidine synthase, speE, is reversible, catalyzing the breakdown of spermidine and norspermidine, in addition to its usual biosynthetic role. These findings provide support for the hypothesis that enzyme multifunctionality enables streamlined cells in planktonic ecosystems to increase the range of DOM compounds they metabolize.

Highlights

In the ocean surface layer and cell culture, the polyamine transport protein PotD of SAR11 bacteria is often one of the most abundant proteins detected
We focused on five polyamine compounds (Table 1), putrescine (PUT), cadaverine (CAD), agmatine (AGM), norspermidine (NSD), and spermidine (SPD)
A collision energy of 20 eV was used for all analytes except 1,3-diaminopropane, which had a CE of 10 eV, and homospermidine, which had a CE of 30 eV. bThe first listed product m/z was used for quantification; the second was used for verification

Summary

Introduction

In the ocean surface layer and cell culture, the polyamine transport protein PotD of SAR11 bacteria is often one of the most abundant proteins detected. Metabolic footprinting and fingerprinting were used to measure the uptake of five polyamine compounds (putrescine, cadaverine, agmatine, norspermidine, and spermidine) in two SAR11 strains that represent the majority of SAR11 cells in the surface ocean environment, “Candidatus Pelagibacter” strain HTCC7211 and “Candidatus Pelagibacter ubique” strain HTCC1062 Both strains took up all five polyamines and concentrated them to micromolar or millimolar intracellular concentrations. Our data suggest that potABCD transports all five polyamines and that spermidine synthase, speE, is reversible, catalyzing the breakdown of spermidine and norspermidine, in addition to its usual biosynthetic role These findings provide support for the hypothesis that enzyme multifunctionality enables streamlined cells in planktonic ecosystems to increase the range of DOM compounds they metabolize.

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