Why microbes secrete molecules to modify their environment: the case of iron-chelating siderophores

Leventhal, Gabriel E.; Ackermann, Martin; Schiessl, Konstanze T.

doi:10.1098/rsif.2018.0674

Cited by 68 publications

(70 citation statements)

References 72 publications

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“…CM in both clots and coatings likely consists of intermixed cellular material reflecting a metabolic network or biocoenosis 14,31 , together with extracellular biomolecules and metal-chelating proteins, both of which contain anions (cell proteins and aspartic and glutamic acids) able to chelate metal cations, for example Cu 33,69 . Significant metal accumulation associated with potential siderophores and other highly chelating proteins 70 not of direct relevance to the metallome would have been removed with minerals (i.e., point sources of extreme enrichment; Figs. 2e,f, S4-S8) during spatial quantification (see methods described in Supplementary Material) and would not hinder the distinction of metal accumulation within CM itself.…”

Section: Origin Of the Palaeo-metallomic Biosignaturementioning

confidence: 99%

“…This exceptional elemental complement alone is strong evidence for this CM having a biogenic origin. V is considered either bio-essential or bio-functional 40,70 and has high retention potential within CM 62 . Very high fractional contributions of V in clots and coatings may stem from this preferential retention or original enrichment and, while potentially an overestimate relative to enrichments in other elements, suggests metabolic contributions from methanotrophic and diazotrophic organisms 23,41 .…”

Section: Metabolism Of the Precursor Biomassmentioning

confidence: 99%

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Metallomics in deep time and the influence of ocean chemistry on the metabolic landscapes of Earth’s earliest ecosystems

Hickman‐Lewis

Cavalazzi

Sorieul

et al. 2020

Sci Rep

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Modern biological dependency on trace elements is proposed to be a consequence of their enrichment in the habitats of early life together with Earth's evolving physicochemical conditions; the resulting metallic biological complement is termed the metallome. Herein, we detail a protocol for describing metallomes in deep time, with applications to the earliest fossil record. Our approach extends the metallome record by more than 3 Ga and provides a novel, non-destructive method of estimating biogenicity in the absence of cellular preservation. Using microbeam particle-induced X-ray emission (µPIXE), we spatially quantify transition metals and metalloids within organic material from 3.33 billionyear-old cherts of the Barberton greenstone belt, and demonstrate that elements key to anaerobic prokaryotic molecular nanomachines, including Fe, V, Ni, As and Co, are enriched within carbonaceous material. Moreover, Mo and Zn, likely incorporated into enzymes only after the Great Oxygenation Event, are either absent or present at concentrations below the limit of detection of µPIXE, suggesting minor biological utilisation in this environmental setting. Scanning and transmission electron microscopy demonstrates that metal enrichments do not arise from accumulation in nanomineral phases and thus unambiguously reflect the primary composition of the carbonaceous material. This carbonaceous material also has δ 13 c between −41.3‰ and 0.03‰, dominantly −21.0‰ to −11.5‰, consistent with biological fractionation and mostly within a restricted range inconsistent with abiotic processes. Considering spatially quantified trace metal enrichments and negative δ 13 C fractionations together, we propose that, although lacking cellular preservation, this organic material has biological origins and, moreover, that its precursor metabolism may be estimated from the fossilised "palaeometallome". Enriched Fe, V, Ni and Co, together with petrographic context, suggests that this kerogen reflects the remnants of a lithotrophic or organotrophic consortium cycling methane or nitrogen. Palaeo-metallome compositions could be used to deduce the metabolic networks of Earth's earliest ecosystems and, potentially, as a biosignature for evaluating the origin of preserved organic materials found on Mars.

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Section: Origin Of the Palaeo-metallomic Biosignaturementioning

confidence: 99%

Section: Metabolism Of the Precursor Biomassmentioning

confidence: 99%

Metallomics in deep time and the influence of ocean chemistry on the metabolic landscapes of Earth’s earliest ecosystems

Hickman‐Lewis

Cavalazzi

Sorieul

et al. 2020

Sci Rep

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“…Particulate organic matter (POM) provides a scaffold for cells to attach to and grow in close proximity, increasing the opportunity for microbial interactions to take place (11). A particularly relevant type of interaction in this context is cell–cell cooperation, in which cells mutually benefit from being close to each other by increasing the availability of public goods such as extracellular hydrolysis products (12–14). Although numerous studies have demonstrated that this type of interaction can occur both in the laboratory and in nature, we lack a quantitative understanding of the conditions in which cooperation takes place in an environment such as the ocean, and how it can affect bacterially mediated functions such as the turnover of POM.…”

mentioning

confidence: 99%

Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria

Ebrahimi

Schwartzman

Cordero

2019

Proc. Natl. Acad. Sci. U.S.A.

118

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The recycling of particulate organic matter (POM) by microbes is a key part of the global carbon cycle. This process is mediated by the extracellular hydrolysis of polysaccharides, which can trigger social behaviors in bacteria resulting from the production of public goods. Despite the potential importance of public good-mediated interactions, their relevance in the environment remains unclear. In this study, we developed a computational and experimental model system to address this challenge and studied how the POM depolymerization rate and its uptake efficiency (2 main ecosystem function parameters) depended on social interactions and spatial self-organization on particle surfaces. We found an emergent trade-off between rate and efficiency resulting from the competition between oligosaccharide diffusion and cellular uptake, with low rate and high efficiency being achieved through cell-to-cell cooperation between degraders. Bacteria cooperated by aggregating in cell clusters of ∼10 to 20 µm, in which cells were able to share public goods. This phenomenon, which was independent of any explicit group-level regulation, led to the emergence of critical cell concentrations below which degradation did not occur, despite all resources being available in excess. In contrast, when particles were labile and turnover rates were high, aggregation promoted competition and decreased the efficiency of carbon use. Our study shows how social interactions and cell aggregation determine the rate and efficiency of particulate carbon turnover in environmentally relevant scenarios.

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“…Ecological complexity in the microbial world stems from chemical interactions. Microbes engage in every conceivable form of biotic interaction, ranging from intraspecific and interspecific competition (61, 62) to predation (63, 64), to a variety of cooperative interactions that encompass communal feeding (65,66), to detoxification of growth-inhibitory compounds (67), and to cross-feeding (68,69). Played out against a backdrop of spatiotemporal variation in abiotic factors such as pH, redox potential, pO 2 , inorganic ions, light, and temperature (70-77), biotic interactions give rise to the structure and dynamics of microbial communities in nature.…”

Section: Discussionmentioning

confidence: 99%

Fitness and Productivity Increase with Ecotypic Diversity among Escherichia coli Strains That Coevolved in a Simple, Constant Environment

Yang

Alexander

Kinnersley

et al. 2020

Appl Environ Microbiol

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The productivity of a biological community often correlates with its diversity. In the microbial world this phenomenon can sometimes be explained by positive, density-dependent interactions such as cross-feeding and syntrophy. These metabolic interactions help account for the astonishing variety of microbial life and drive many of the biogeochemical cycles without which life as we know it could not exist. While it is difficult to recapitulate experimentally how these interactions evolved among multiple taxa, we can explore in the laboratory how they arise within one. These experiments provide insight into how different bacterial ecotypes evolve and from these, possibly new “species.” We have previously shown that in a simple, constant environment a single clone of Escherichia coli can give rise to a consortium of genetically and phenotypically differentiated strains, in effect, a set of ecotypes, that coexist by cross-feeding. We marked these different ecotypes and their shared ancestor by integrating fluorescent protein into their genomes and then used flow cytometry to show that each evolved strain is more fit than the shared ancestor, that pairs of evolved strains are fitter still, and that the entire consortium is the fittest of all. We further demonstrate that the rank order of fitness values agrees with estimates of yield, indicating that an experimentally evolved consortium more efficiently converts primary and secondary resources to offspring than its ancestor or any member acting in isolation. IMPORTANCE Polymicrobial consortia occur in both environmental and clinical settings. In many cases, diversity and productivity correlate in these consortia, especially when sustained by positive, density-dependent interactions. However, the evolutionary history of such entities is typically obscure, making it difficult to establish the relative fitness of consortium partners and to use those data to illuminate the diversity-productivity relationship. Here, we dissect an Escherichia coli consortium that evolved under continuous glucose limitation in the laboratory from a single common ancestor. We show that a partnership consisting of cross-feeding ecotypes is better able to secure primary and secondary resources and to convert those resources to offspring than the ancestral clone. Such interactions may be a prelude to a special form of syntrophy and are likely determinants of microbial community structure in nature, including those having clinical significance such as chronic infections.

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Why microbes secrete molecules to modify their environment: the case of iron-chelating siderophores

Cited by 68 publications

References 72 publications

Metallomics in deep time and the influence of ocean chemistry on the metabolic landscapes of Earth’s earliest ecosystems

Metallomics in deep time and the influence of ocean chemistry on the metabolic landscapes of Earth’s earliest ecosystems

Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria

Fitness and Productivity Increase with Ecotypic Diversity among Escherichia coli Strains That Coevolved in a Simple, Constant Environment

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