SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter

Abstract

Summary Marine bacterioplankton face stiff competition for limited nutrient resources. SAR11, a ubiquitous clade of very small and highly abundant Alphaproteobacteria, are known to devote much of their energy to synthesizing ATP‐binding cassette periplasmic proteins that bind substrates. We hypothesized that their small size and relatively large periplasmic space might enable them to outcompete other bacterioplankton for nutrients. Using uptake experiments with 14C‐glycine betaine, we discovered that two strains of SAR11, Candidatus Pelagibacter sp. HTCC7211 and Cand. P. ubique HTCC1062, have extraordinarily high affinity for glycine betaine (GBT), with half‐saturation (K s) values around 1 nM and specific affinity values between 8 and 14 L mg cell−1 h−1. Competitive inhibition studies indicated that the GBT transporters in these strains are multifunctional, transporting multiple substrates in addition to GBT. Both strains could use most of the transported compounds for metabolism and ATP production. Our findings indicate that Pelagibacter cells are primarily responsible for the high affinity and multifunctional GBT uptake systems observed in seawater. Maximization of whole‐cell affinities may enable these organisms to compete effectively for nutrients during periods when the gross transport capacity of the heterotrophic plankton community exceeds the supply, depressing ambient concentrations.

Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria

“…Michaelis-Menten formulation of transport and to the traditional assumption that the value of / for ABC transport is a constant that is intrinsic to the binding proteins (Button, 1998;Noell & Giovannoni, 2019). Instead, we find that / depends on both the dissociation constant of the substrate and binding protein ( 6 ) and the dissociation constant of the resulting complex and the transport unit ( ′ ' ).…”

“…coli's similar glycine betaine transport system uses a binding protein with a dissociation constant in the micromolar regime (Noell & Giovannoni, 2019). Our model shows that a nanomolarcan be achieved by a cell using a binding protein with a micromolar 6 , if the cell has abundant binding proteins.…”

“…Genomic analyses suggest that the divergent phenotypic traits of copiotrophs and oligotrophs are correlated with their suite of genes for nutrient transport (Lauro et al, 2009;Sowell et al, 2009;Cottrell & Kirchman, 2016;Noell & Giovannoni, 2019). Copiotrophs have many genes for phosphotransferase systems (PTS) used to uptake specific sugars (Kotrba et al, 2001).…”

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

“…The MWH suite of media was modified from the JW media to additionally include choline, glycerol, glycine betaine, cyanate, DMSO, DMSP, thiosulfate, and orthophosphate. These compounds have been identified as important metabolites and osmolytes for marine and freshwater prokaryotes and were absent in the first iteration (JW) of our media (Table S1) (88–94). A total of 1,463 wells were positive (> 10 4 cells ·ml -1 ), and 738 of these were transferred to 125 mL polycarbonate flasks.…”

Influence of Substrate Concentration on the Culturability of Heterotrophic Soil Microbes Isolated by High-Throughput Dilution-to-Extinction Cultivation

“…These "streamlined" genomes often code for fewer copies of the rRNA gene operon and transcriptional regulator genes than microbes with larger genomes, suggesting that oligotrophs lack the ability to sense and rapidly respond to variable environmental conditions (12,16,92). Instead, genomic inventories of marine oligotrophs suggest a reliance on broad-specificity, high-affinity transporters that are constitutively expressed (22,(26)(27)(28).…”