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

2020 ◽  
Author(s):  
Noele Norris ◽  
Naomi M. Levine ◽  
Vicente I. Fernandez ◽  
Roman Stocker
Keyword(s):  
Nutrient Uptake ◽  
Binding Proteins ◽  
Heterotrophic Bacteria ◽  
Dissociation Constants ◽  
Mechanistic Model ◽  
Divergent Evolution ◽  
Abc Transport ◽  
Trade Offs ◽  
Marine Heterotrophic Bacteria ◽  
Level Model

AbstractMarine heterotrophic bacteria use a spectrum of nutrient uptake strategies, from that of copiotrophs—which dominate in nutrient-rich environments—to that of oligotrophs—which dominate in nutrient-poor environments. While copiotrophs possess numerous phosphotransferase systems (PTS), oligotrophs lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. Here we present a molecular-level model that explains the dichotomy between oligotrophs and copiotrophs as the consequence of trade-offs between PTS and ABC transport. When we approximate ABC transport in Michaelis–Menten form, we find, contrary to the canonical formulation, that its half-saturation concentration KM is not a constant but instead a function of binding protein abundance. Thus, oligotrophs can attain nanomolar KM values using binding proteins with micromolar dissociation constants and while closely matching transport and metabolic capacities. However, this requires large periplasms and high abundances of binding proteins, whose slow diffusion limits uptake rate. We conclude that the use of binding proteins is critical for oligotrophic survival yet severely constrains maximal growth rates, thus fundamentally shaping the divergent evolution of oligotrophs and copiotrophs.

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

2021 ◽  
Vol 17 (5) ◽  
pp. e1009023
Author(s):  
Noele Norris ◽  
Naomi M. Levine ◽  
Vicente I. Fernandez ◽  
Roman Stocker
Keyword(s):  
Nutrient Uptake ◽  
Binding Proteins ◽  
Dissociation Constants ◽  
Mechanistic Model ◽  
Cell Metabolism ◽  
Transport Systems ◽  
Divergent Evolution ◽  
Trade Offs ◽  
Level Model ◽  
Metabolic Strategies

Marine bacterial diversity is immense and believed to be driven in part by trade-offs in metabolic strategies. Here we consider heterotrophs that rely on organic carbon as an energy source and present a molecular-level model of cell metabolism that explains the dichotomy between copiotrophs—which dominate in carbon-rich environments—and oligotrophs—which dominate in carbon-poor environments—as the consequence of trade-offs between nutrient transport systems. While prototypical copiotrophs, like Vibrios, possess numerous phosphotransferase systems (PTS), prototypical oligotrophs, such as SAR11, lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. We develop models of both transport systems and use them in proteome allocation problems to predict the optimal nutrient uptake and metabolic strategy as a function of carbon availability. We derive a Michaelis–Menten approximation of ABC transport, analytically demonstrating how the half-saturation concentration is a function of binding protein abundance. We predict that oligotrophs can attain nanomolar half-saturation concentrations using binding proteins with only micromolar dissociation constants and while closely matching transport and metabolic capacities. However, our model predicts that this requires large periplasms and that the slow diffusion of the binding proteins limits uptake. Thus, binding proteins are critical for oligotrophic survival yet severely constrain growth rates. We propose that this trade-off fundamentally shaped the divergent evolution of oligotrophs and copiotrophs.

scholarly journals Contingent evolution of alternative metabolic network topologies determines whether cross-feeding evolves

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Jeroen Meijer ◽  
Bram van Dijk ◽  
Paulien Hogeweg
Keyword(s):  
Metabolic Networks ◽  
Mechanistic Model ◽  
Building Blocks ◽  
Division Of Labour ◽  
Ecosystem Structure ◽  
Evolutionary Contingency ◽  
Trade Offs ◽  
Evolutionary Trajectories ◽  
Network Topologies ◽  
Metabolic Strategies

AbstractMetabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Here we use a mechanistic model to study how metabolic strategies evolve in a constant, one resource environment, when metabolic networks are allowed to freely evolve. We find that initially identical ancestral communities of digital organisms follow different evolutionary trajectories, as some communities become dominated by a single, autonomous lineage, while others are formed by stably coexisting lineages that cross-feed on essential building blocks. Our results show how without presupposed cellular trade-offs or external drivers such as temporal niches, diverse metabolic strategies spontaneously emerge from the interplay between ecology, spatial structure, and metabolic constraints that arise during the evolution of metabolic networks. Thus, in the long term, whether microbes remain autonomous or evolve metabolic division of labour is an evolutionary contingency.

scholarly journals Structure-Function Analysis Indicates that an Active-Site Water Molecule Participates in Dimethylsulfoniopropionate Cleavage by DddK

2019 ◽  
Vol 85 (8) ◽  
Author(s):  
Ming Peng ◽  
Xiu-Lan Chen ◽  
Dian Zhang ◽  
Xiu-Juan Wang ◽  
Ning Wang ◽  
...  
Keyword(s):  
Water Molecule ◽  
Active Site ◽  
Dimethyl Sulfide ◽  
Catalytic Mechanism ◽  
Heterotrophic Bacteria ◽  
Function Analysis ◽  
Cloud Condensation Nuclei ◽  
Oxidation Products ◽  
Condensation Nuclei ◽  
Marine Heterotrophic Bacteria

ABSTRACT The osmolyte dimethylsulfoniopropionate (DMSP) is produced in petagram quantities in marine environments and has important roles in global sulfur and carbon cycling. Many marine microorganisms catabolize DMSP via DMSP lyases, generating the climate-active gas dimethyl sulfide (DMS). DMS oxidation products participate in forming cloud condensation nuclei and, thus, may influence weather and climate. SAR11 bacteria are the most abundant marine heterotrophic bacteria; many of them contain the DMSP lyase DddK, and their dddK transcripts are relatively abundant in seawater. In a recently described catalytic mechanism for DddK, Tyr64 is predicted to act as the catalytic base initiating the β-elimination reaction of DMSP. Tyr64 was proposed to be deprotonated by coordination to the metal cofactor or its neighboring His96. To further probe this mechanism, we purified and characterized the DddK protein from Pelagibacter ubique strain HTCC1062 and determined the crystal structures of wild-type DddK and its Y64A and Y122A mutants (bearing a change of Y to A at position 64 or 122, respectively), where the Y122A mutant is complexed with DMSP. The structural and mutational analyses largely support the catalytic role of Tyr64, but not the method of its deprotonation. Our data indicate that an active water molecule in the active site of DddK plays an important role in the deprotonation of Tyr64 and that this is far more likely than coordination to the metal or His96. Sequence alignment and phylogenetic analysis suggest that the proposed catalytic mechanism of DddK has universal significance. Our results provide new mechanistic insights into DddK and enrich our understanding of DMS generation by SAR11 bacteria. IMPORTANCE The climate-active gas dimethyl sulfide (DMS) plays an important role in global sulfur cycling and atmospheric chemistry. DMS is mainly produced through the bacterial cleavage of marine dimethylsulfoniopropionate (DMSP). When released into the atmosphere from the oceans, DMS can be photochemically oxidized into DMSO or sulfate aerosols, which form cloud condensation nuclei that influence the reflectivity of clouds and, thereby, global temperature. SAR11 bacteria are the most abundant marine heterotrophic bacteria, and many of them contain DMSP lyase DddK to cleave DMSP, generating DMS. In this study, based on structural analyses and mutational assays, we revealed the catalytic mechanism of DddK, which has universal significance in SAR11 bacteria. This study provides new insights into the catalytic mechanism of DddK, leading to a better understanding of how SAR11 bacteria generate DMS.

scholarly journals Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacteria: example of the model algae-associated bacteriumZobellia galactanivoransDsijT

2016 ◽  
Vol 18 (12) ◽  
pp. 4610-4627 ◽  
Author(s):  
Tristan Barbeyron ◽  
François Thomas ◽  
Valérie Barbe ◽  
Hanno Teeling ◽  
Chantal Schenowitz ◽  
...  
Keyword(s):  
Heterotrophic Bacteria ◽  
Driving Forces ◽  
Marine Heterotrophic Bacteria ◽  
Carbohydrate Catabolism

scholarly journals Facilitation of Robust Growth of Prochlorococcus Colonies and Dilute Liquid Cultures by “Helper” Heterotrophic Bacteria

2008 ◽  
Vol 74 (14) ◽  
pp. 4530-4534 ◽  
Author(s):  
J. Jeffrey Morris ◽  
Robin Kirkegaard ◽  
Martin J. Szul ◽  
Zackary I. Johnson ◽  
Erik R. Zinser
Keyword(s):  
Solid Medium ◽  
Heterotrophic Bacteria ◽  
Cell Concentration ◽  
Preliminary Evidence ◽  
Critical Threshold ◽  
Semisolid Medium ◽  
Marine Heterotrophic Bacteria ◽  
Pure Cultures ◽  
Novel Method ◽  
Axenic Cultures

ABSTRACT Axenic (pure) cultures of marine unicellular cyanobacteria of the Prochlorococcus genus grow efficiently only if the inoculation concentration is large; colonies form on semisolid medium at low efficiencies. In this work, we describe a novel method for growing Prochlorococcus colonies on semisolid agar that improves the level of recovery to approximately 100%. Prochlorococcus grows robustly at low cell concentrations, in liquid or on solid medium, when cocultured with marine heterotrophic bacteria. Once the Prochlorococcus cell concentration surpasses a critical threshold, the “helper” heterotrophs can be eliminated with antibiotics to produce axenic cultures. Our preliminary evidence suggests that one mechanism by which the heterotrophs help Prochlorococcus is the reduction of oxidative stress.

scholarly journals The Mannitol Utilization System of the Marine Bacterium Zobellia galactanivorans

2014 ◽  
Vol 81 (5) ◽  
pp. 1799-1812 ◽  
Author(s):  
Agnès Groisillier ◽  
Aurore Labourel ◽  
Gurvan Michel ◽  
Thierry Tonon
Keyword(s):  
Abc Transporter ◽  
Biochemical Characterization ◽  
Heterotrophic Bacteria ◽  
Dry Weight ◽  
Sole Source ◽  
Content Type ◽  
Wide Range ◽  
Marine Heterotrophic Bacteria ◽  
Operon Gene ◽  
Living Organisms

ABSTRACTMannitol is a polyol that occurs in a wide range of living organisms, where it fulfills different physiological roles. In particular, mannitol can account for as much as 20 to 30% of the dry weight of brown algae and is likely to be an important source of carbon for marine heterotrophic bacteria.Zobellia galactanivorans(Flavobacteriia) is a model for the study of pathways involved in the degradation of seaweed carbohydrates. Annotation of its genome revealed the presence of genes potentially involved in mannitol catabolism, and we describe here the biochemical characterization of a recombinant mannitol-2-dehydrogenase (M2DH) and a fructokinase (FK). Among the observations, the M2DH ofZ. galactanivoranswas active as a monomer, did not require metal ions for catalysis, and featured a narrow substrate specificity. The FK characterized was active on fructose and mannose in the presence of a monocation, preferentially K+. Furthermore, the genes coding for these two proteins were adjacent in the genome and were located directly downstream of three loci likely to encode an ATP binding cassette (ABC) transporter complex, suggesting organization into an operon. Gene expression analysis supported this hypothesis and showed the induction of these five genes after culture ofZ. galactanivoransin the presence of mannitol as the sole source of carbon. This operon for mannitol catabolism was identified in only 6 genomes ofFlavobacteriaceaeamong the 76 publicly available at the time of the analysis. It is not conserved in allBacteroidetes; some species contain a predicted mannitol permease instead of a putative ABC transporter complex upstream of M2DH and FK ortholog genes.

scholarly journals Metabolic strategies of sharing pioneer bacteria mediating fresh macroalgae breakdown

2021 ◽  
Author(s):  
Maéva Brunet ◽  
Nolwen Le Duff ◽  
Tristan Barbeyron ◽  
François Thomas
Keyword(s):  
Extracellular Enzymes ◽  
Heterotrophic Bacteria ◽  
Physical Contact ◽  
Brown Macroalgae ◽  
Resistance Proteins ◽  
Biomass Turnover ◽  
Macroalgal Biomass ◽  
Marine Heterotrophic Bacteria ◽  
Metabolic Strategies ◽  
Polysaccharide Utilization Loci

Macroalgae represent huge amounts of biomass worldwide, largely recycled by marine heterotrophic bacteria. We investigated the strategies of pioneer bacteria within the flavobacterial genus Zobellia to initiate the degradation of fresh brown macroalgae, which has received little attention compared to the degradation of isolated polysaccharides. Zobellia galactanivorans DsijT could use macroalgae as a sole carbon source and extensively degrade algal tissues without requiring physical contact, via the secretion of extracellular enzymes. This indicated a sharing behaviour, whereby pioneers release public goods that can fuel other bacteria. Comparisons of eight Zobellia strains, and strong transcriptomic shifts in Z. galactanivorans cells using fresh macroalgae vs. isolated polysaccharides, revealed potential overlooked traits of pioneer bacteria. Besides brown algal polysaccharide degradation, they notably include stress resistance proteins, type IX secretion system proteins and novel uncharacterized Polysaccharide Utilization Loci. Overall, this work highlights the relevance of studying fresh macroalga degradation to fully understand the niche, metabolism and evolution of pioneer degraders, as well as their cooperative interactions within microbial communities, as key players in macroalgal biomass turnover.

scholarly journals A mechanistic link between cellular trade-offs, gene expression and growth

2015 ◽  
Author(s):  
Andrea Y. Weisse ◽  
Diego A. Oyarzun ◽  
Vincent Danos ◽  
Peter S. Swain
Keyword(s):  
Gene Expression ◽  
Growth Rate ◽  
Metabolic Pathways ◽  
Mechanistic Model ◽  
Living Cells ◽  
Coarse Grained ◽  
Empirical Relationships ◽  
Cellular Energy ◽  
Modelling Framework ◽  
Trade Offs

Intracellular processes rarely work in isolation but continually interact with the rest of the cell. In microbes, for example, we now know that gene expression across the whole genome typically changes with growth rate. The mechanisms driving such global regulation, however, are not well understood. Here we consider three trade-offs that because of limitations in levels of cellular energy, free ribosomes, and proteins are faced by all living cells and construct a mechanistic model that comprises these trade-offs. Our model couples gene expression with growth rate and growth rate with a growing population of cells. We show that the model recovers Monod's law for the growth of microbes and two other empirical relationships connecting growth rate to the mass fraction of ribosomes. Further, we can explain growth related effects in dosage compensation by paralogs and predict host-circuit interactions in synthetic biology. Simulating competitions between strains, we find that the regulation of metabolic pathways may have evolved not to match expression of enzymes to levels of extracellular substrates in changing environments but rather to balance a trade-off between exploiting one type of nutrient over another. Although coarse-grained, the trade-offs that the model embodies are fundamental, and, as such, our modelling framework has potentially wide application, including in both biotechnology and medicine.

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