Spatial metabolomics of in situ host–microbe interactions at the micrometre scale

Geier, Benedikt; Sogin, Emilia M.; Michellod, Dolma; Janda, Moritz; Kompauer, Mario; Spengler, Bernhard; Dubilier, Nicole; Liebeke, Manuel

doi:10.1038/s41564-019-0664-6

Cited by 156 publications

(132 citation statements)

References 85 publications

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“…65 Increased emphasis on studying immune cell metabolism in vivo, or in more sophisticated culture systems such as those provided by organoids, 107,108 is therefore warranted. In this general context, the application of advances in single-cell metabolomics 109 and spatial metabolomics [110][111][112][113] has the potential to greatly improve the resolution of future studies.…”

Section: Future Pros Pec Tsmentioning

confidence: 99%

Cell‐intrinsic metabolic regulation of mononuclear phagocyte activation: Findings from the tip of the iceberg

Bakker

Pearce

2020

Immunological Reviews

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We have only recently started to appreciate the extent to which immune cell activation involves significant changes in cellular metabolism. We are now beginning to understand how commitment to specific metabolic pathways influences aspects of cellular biology that are the more usual focus of immunological studies, such as activation-induced changes in gene transcription, post-transcriptional regulation of transcription, post-translational modifications of proteins, cytokine secretion, etc. Here, we focus on metabolic reprogramming in mononuclear phagocytes downstream of stimulation with inflammatory signals (such as LPS and IFNγ) vs alternative activation signals (IL-4), with an emphasis on work on dendritic cells and macrophages from our laboratory, and related studies from others. We cover aspects of glycolysis and its branching pathways (glycogen synthesis, pentose phosphate, serine synthesis, hexose synthesis, and glycerol 3 phosphate shuttle), the tricarboxylic acid pathway, fatty acid synthesis and oxidation, and mitochondrial biology. Although our understanding of the metabolism of mononuclear phagocytes has progressed significantly over the last 10 years, major challenges remain, including understanding the effects of tissue residence on metabolic programming related to cellular activation, and the translatability of findings from mouse to human biology. K E Y W O R D SThis is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Section: Future Pros Pec Tsmentioning

confidence: 99%

Cell‐intrinsic metabolic regulation of mononuclear phagocyte activation: Findings from the tip of the iceberg

Bakker

Pearce

2020

Immunological Reviews

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“…S-3). After MALDI-TOF-MSI we used bright-field microscopy and fluorescence in situ hybridization (FISH) to image the histology and the bacteria in each of the four tissue sections (10)(Fig. 2 and SI Appendix , Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The sum of mutualistic, commensal and pathogenic interactions results in a unique anatomic and in particular, metabolic phenotype for nearly every host individual (9). The ability to connect metabolic with anatomic phenotypes of host and symbiont tissues in the same host animal could allow us to disentangle how the interactions between the symbiotic partners affect metabolic heterogeneity (10). Previous studies have addressed this methodological challenge by combining non-destructive magnet resonance tomography (MRT) with matrix-assisted laser desorption/ionization (MALDI)-MSI to connect the spatial chemistry and 3D anatomy of organs (11) and pathogenic abscesses (12, 13) of the same animals.…”

Section: Introductionmentioning

confidence: 99%

Connecting structure and function from organisms to molecules in small animal symbioses through chemo-histo-tomography

Geier

Oetjen

Ruthensteiner

et al. 2020

Preprint

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Our understanding of the metabolites involved in the interactions between small symbiotic animals and bacteria or other eukaryotes that reside within their body is extremely limited. This gap in knowledge originates from a methodological challenge, namely to connect metabolites to the histological changes in host tissues throughout colonization and persistence of beneficial and parasitic (micro)organisms in situ. To close this gap, we developed chemo-histo-tomography (CHEMHIST), a culture-independent approach to connect anatomic structure and metabolic function in millimeter-sized symbiotic animals. CHEMHIST combines spatial metabolomics based on mass spectrometry imaging (MSI) and microanatomy-based micro-computed X-ray tomography (microCT) on the same animal. Both high-resolution MSI and microCT allowed us to correlate the distribution of metabolites to the same animals three-dimensional (3D) histology down to sub-micrometer resolutions. Building CHEMHIST upon in situ imaging approaches, we sampled an earthworm from its natural habitat and created an interactive 3D model of its physical and chemical interactions with bacteria and parasitic nematodes in its tissues. Our CHEMHIST protocol is compatible with other molecular techniques, which include tissue specific DNA sequencing and localization of bacteria using fluorescence in situ hybridization (FISH) to complement the spatial metabolomics data. We demonstrate on an earthworm, a key species for soil ecosystem-functioning across the globe that combining MSI and microCT offers a powerful platform to connect metabolic and anatomic phenotypes of small symbiotic animals in situ.

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“…This type of symbiosis between animals and chemolithoautotrophic microbes is very common, not only in unusual environments like hydrothermal vents (where geothermally heated water and gases escape from fissures) and cold seeps (where the efflux is more diffuse and cooler than in hydrothermal vents), but also more normal environments like intertidal marine sediments (Dubilier et al , 2008). New techniques provide unprecedented visual insight at the micrometre scale into such host–microbe symbioses and their metabolic interactions (Geier et al , 2020). Photographs A and B by Terry McGenity and C by MARUM – Center for Marine Environmental Sciences, University of Bremen (CC‐BY 4.0).…”

Section: Importing Excursions Into School and Virtual Excursionsmentioning

confidence: 99%

Visualizing the invisible: class excursions to ignite children’s enthusiasm for microbes

McGenity

Gessesse

Hallsworth

et al. 2020

Microbial Biotechnology

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Summary We have recently argued that, because microbes have pervasive – often vital – influences on our lives, and that therefore their roles must be taken into account in many of the decisions we face, society must become microbiology‐literate, through the introduction of relevant microbiology topics in school curricula (Timmis et al. 2019. Environ Microbiol 21: 1513‐1528). The current coronavirus pandemic is a stark example of why microbiology literacy is such a crucial enabler of informed policy decisions, particularly those involving preparedness of public‐health systems for disease outbreaks and pandemics. However, a significant barrier to attaining widespread appreciation of microbial contributions to our well‐being and that of the planet is the fact that microbes are seldom visible: most people are only peripherally aware of them, except when they fall ill with an infection. And it is disease, rather than all of the positive activities mediated by microbes, that colours public perception of ‘germs’ and endows them with their poor image. It is imperative to render microbes visible, to give them life and form for children (and adults), and to counter prevalent misconceptions, through exposure to imagination‐capturing images of microbes and examples of their beneficial outputs, accompanied by a balanced narrative. This will engender automatic mental associations between everyday information inputs, as well as visual, olfactory and tactile experiences, on the one hand, and the responsible microbes/microbial communities, on the other hand. Such associations, in turn, will promote awareness of microbes and of the many positive and vital consequences of their actions, and facilitate and encourage incorporation of such consequences into relevant decision‐making processes. While teaching microbiology topics in primary and secondary school is key to this objective, a strategic programme to expose children directly and personally to natural and managed microbial processes, and the results of their actions, through carefully planned class excursions to local venues, can be instrumental in bringing microbes to life for children and, collaterally, their families. In order to encourage the embedding of microbiology‐centric class excursions in current curricula, we suggest and illustrate here some possibilities relating to the topics of food (a favourite pre‐occupation of most children), agriculture (together with horticulture and aquaculture), health and medicine, the environment and biotechnology. And, although not all of the microbially relevant infrastructure will be within reach of schools, there is usually access to a market, local food store, wastewater treatment plant, farm, surface water body, etc., all of which can provide opportunities to explore microbiology in action. If children sometimes consider the present to be mundane, even boring, they are usually excited with both the past and the future so, where possible, visits to local museums (the past) and research institutions advancing knowledge frontiers (the...

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Spatial metabolomics of in situ host–microbe interactions at the micrometre scale

Cited by 156 publications

References 85 publications

Cell‐intrinsic metabolic regulation of mononuclear phagocyte activation: Findings from the tip of the iceberg

Cell‐intrinsic metabolic regulation of mononuclear phagocyte activation: Findings from the tip of the iceberg

Connecting structure and function from organisms to molecules in small animal symbioses through chemo-histo-tomography

Visualizing the invisible: class excursions to ignite children’s enthusiasm for microbes

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