Christopher Field

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Field

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Christopher

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0000-0002-6434-3745

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Publications 1 - 10 of 16

Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome
Salazar Guiral, Guillem; Paoli, Lucas Pierre Antoine; Alberti, Adriana; et al. (2019)
Cell
Ocean microbial communities strongly influence the biogeochemistry, food webs, and climate of our planet. Despite recent advances in understanding their taxonomic and genomic compositions, little is known about how their transcriptomes vary globally. Here, we present a dataset of 187 metatranscriptomes and 370 metagenomes from 126 globally distributed sampling stations and establish a resource of 47 million genes to study community-level transcriptomes across depth layers from pole-to-pole. We examine gene expression changes and community turnover as the underlying mechanisms shaping community transcriptomes along these axes of environmental variation and show how their individual contributions differ for multiple biogeochemically relevant processes. Furthermore, we find the relative contribution of gene expression changes to be significantly lower in polar than in non-polar waters and hypothesize that in polar regions, alterations in community activity in response to ocean warming will be driven more strongly by changes in organismal composition than by gene regulatory mechanisms.
Genome sequences of Rhizopogon roseolus, Mariannaea elegans, Myrothecium verrucaria, and Sphaerostilbella broomeana and the identification of biosynthetic gene clusters for fungal peptide natural products
Vogt, Eva; Field, Christopher; Sonderegger, Lukas; et al. (2022)
G3: Genes, Genomes, Genetics
In recent years, a variety of fungal cyclic peptides with interesting bioactivities have been discovered. For many of these peptides, the biosynthetic pathways are unknown and their elucidation often holds surprises. The cyclic and backbone N-methylated omphalotins from Omphalotus olearius were recently shown to constitute a novel class (borosins) of ribosomally synthesized and posttranslationally modified peptides, members of which are produced by many fungi, including species of the genus Rhizopogon. Other recently discovered fungal peptide macrocycles include the mariannamides from Mariannaea elegans and the backbone N-methylated verrucamides and broomeanamides from Myrothecium verrucaria and Sphaerostilbella broomeana, respectively. Here, we present draft genome sequences of four fungal species Rhizopogon roseolus, Mariannaea elegans, Myrothecium verrucaria, and Sphaerostilbella broomeana. We screened these genomes for precursor proteins or gene clusters involved in the mariannamide, verrucamide, and broomeanamide biosynthesis including a general screen for borosin-producing precursor proteins. While our genomic screen for potential ribosomally synthesized and posttranslationally modified peptide precursor proteins of mariannamides, verrucamides, broomeanamides, and borosins remained unsuccessful, antiSMASH predicted nonribosomal peptide synthase gene clusters that may be responsible for the biosynthesis of mariannamides, verrucamides, and broomeanamides. In M. verrucaria, our antiSMASH search led to a putative NRPS gene cluster with a predicted peptide product of 20 amino acids, including multiple nonproteinogenic isovalines. This cluster likely encodes a member of the peptaibols, an antimicrobial class of peptides previously isolated primarily from the Genus Trichoderma. The nonribosomal peptide synthase gene clusters discovered in our screenings are promising candidates for future research.
Identification, heterologous production and bioactivity of lentinulin A and dendrothelin A, two natural variants of backbone N-methylated peptide macrocycle omphalotin A
Matabaro, Emmanuel; Kaspar, Hannelore; Dahlin, Paul; et al. (2021)
Scientific Reports
Backbone N-methylation and macrocyclization improve the pharmacological properties of peptides by enhancing their proteolytic stability, membrane permeability and target selectivity. Borosins are backbone N-methylated peptide macrocycles derived from a precursor protein which contains a peptide α-N-methyltransferase domain autocatalytically modifying the core peptide located at its C-terminus. Founding members of borosins are the omphalotins from the mushroom Omphalotus olearius (omphalotins A-I) with nine out of 12 L-amino acids being backbone N-methylated. The omphalotin biosynthetic gene cluster codes for the precursor protein OphMA, the protease prolyloligopeptidase OphP and other proteins that are likely to be involved in other post-translational modifications of the peptide. Mining of available fungal genome sequences revealed the existence of highly homologous gene clusters in the basidiomycetes Lentinula edodes and Dendrothele bispora. The respective borosins, referred to as lentinulins and dendrothelins are naturally produced by L. edodes and D. bispora as shown by analysis of respective mycelial extracts. We produced all three homologous peptide natural products by coexpression of OphMA hybrid proteins and OphP in the yeast Pichia pastoris. The recombinant peptides differ in their nematotoxic activity against the plant pathogen Meloidogyne incognita. Our findings pave the way for the production of borosin peptide natural products and their potential application as novel biopharmaceuticals and biopesticides. © 2021, The Author(s).
The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves
Pfeilmeier, Jonas Sebastian; Petti, Gabriella C.; Bortfeld-Miller, Miriam; et al. (2021)
Nature Microbiology
The plant microbiota consists of a multitude of microorganisms that can affect plant health and fitness. However, it is currently unclear how the plant shapes its leaf microbiota and what role the plant immune system plays in this process. Here, we evaluated Arabidopsis thaliana mutants with defects in different parts of the immune system for an altered bacterial community assembly using a gnotobiotic system. While higher-order mutants in receptors that recognize microbial features and in defence hormone signalling showed substantial microbial community alterations, the absence of the plant NADPH oxidase RBOHD caused the most pronounced change in the composition of the leaf microbiota. The rbohD knockout resulted in an enrichment of specific bacteria. Among these, we identified Xanthomonas strains as opportunistic pathogens that colonized wild-type plants asymptomatically but caused disease in rbohD knockout plants. Strain dropout experiments revealed that the lack of RBOHD unlocks the pathogenicity of individual microbiota members driving dysbiosis in rbohD knockout plants. For full protection, healthy plants require both a functional immune system and a microbial community. Our results show that the NADPH oxidase RBOHD is essential for microbiota homeostasis and emphasizes the importance of the plant immune system in controlling the leaf microbiota.
A general non-self response as part of plant immunity
Maier, Benjamin A.; Kiefer, Patrick; Field, Christopher; et al. (2021)
Nature Plants
Plants, like other multicellular lifeforms, are colonized by microorganisms. How plants respond to their microbiota is currently not well understood. We used a phylogenetically diverse set of 39 endogenous bacterial strains from Arabidopsis thaliana leaves to assess host transcriptional and metabolic adaptations to bacterial encounters. We identified a molecular response, which we termed the general non-self response (GNSR) that involves the expression of a core set of 24 genes. The GNSR genes are not only consistently induced by the presence of most strains, they also comprise the most differentially regulated genes across treatments and are predictive of a hierarchical transcriptional reprogramming beyond the GNSR. Using a complementary untargeted metabolomics approach we link the GNSR to the tryptophan-derived secondary metabolism, highlighting the importance of small molecules in plant–microbe interactions. We demonstrate that several of the GNSR genes are required for resistance against the bacterial pathogen Pseudomonas syringae. Our results suggest that the GNSR constitutes a defence adaptation strategy that is consistently elicited by diverse strains from various phyla, contributes to host protection and involves secondary metabolism.
Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere
Carlström, Charlotte I.; Field, Christopher; Bortfeld-Miller, Miriam; et al. (2019)
Nature Ecology & Evolution
Multicellular organisms, including plants, are colonized by microorganisms, some of which are beneficial to growth and health. The assembly rules for establishing plant microbiota are not well understood, and neither is the extent to which their members interact. We conducted drop-out and late introduction experiments by inoculating Arabidopsis thaliana with synthetic communities from a resource of 62 native bacterial strains to test how arrival order shapes community structure. As a read-out we tracked the relative abundance of all strains in the phyllosphere of individual plants. Our results showed that community assembly is historically contingent and subject to priority effects. Missing strains could, to various degrees, invade an already established microbiota, which was itself resistant and remained largely unaffected by latecomers. Additionally, our results indicate that individual strains of Proteobacteria (Sphingomonas, Rhizobium) and Actinobacteria (Microbacterium, Rhodococcus) have the greatest potential to affect community structure as keystone species.
Complex general stress response regulation in Sphingomonas melonis Fr1 revealed by transcriptional analyses
Gottschlich, Lisa; Geiser, Petra; Bortfeld-Miller, Miriam; et al. (2019)
Scientific Reports
The general stress response (GSR) represents an important trait to survive in the environment by leading to multiple stress resistance. In alphaproteobacteria, the GSR is under the transcriptional control of the alternative sigma factor EcfG. Here we performed transcriptome analyses to investigate the genes controlled by EcfG of Sphingomonas melonis Fr1 and the plasticity of this regulation under stress conditions. We found that EcfG regulates genes for proteins that are typically associated with stress responses. Moreover, EcfG controls regulatory proteins, which likely fine-tune the GSR. Among these, we identified a novel negative GSR feedback regulator, termed NepR2, on the basis of gene reporter assays, phenotypic analyses, and biochemical assays. Transcriptional profiling of signaling components upstream of EcfG under complex stress conditions showed an overall congruence with EcfG-regulated genes. Interestingly however, we found that the GSR is transcriptionally linked to the regulation of motility and biofilm formation via the single domain response regulator SdrG and GSR-activating histidine kinases. Altogether, our findings indicate that the GSR in S. melonis Fr1 underlies a complex regulation to optimize resource allocation and resilience in stressful and changing environments.
Inducing novel endosymbioses by implanting bacteria in fungi
Giger, Gabriel H.; Ernst, Chantal; Richter, Ingrid; et al. (2024)
Nature
Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification1,2. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect3-5. Here we implant bacteria into the filamentous fungus Rhizopus microsporus to follow the fate of artificially induced endosymbioses. Whereas Escherichia coli implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis, Mycetohabitans rhizoxinica was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
Author Correction: Identifcation, heterologous production and bioactivity of lentinulin A and dendrothelin A, two natural variants of backbone N-methylated peptide macrocycle omphalotin A
Matabaro, Emmanuel; Kaspar, Hannelore; Dahlin, Paul; et al. (2021)
Scientific Reports
Whole genome phylogenies reflect the distributions of recombination rates for many bacterial species
Sakoparnig, Thomas; Field, Christopher; van Nimwegen, Erik (2021)
eLife
Although recombination is accepted to be common in bacteria, for many species robust phylogenies with well-resolved branches can be reconstructed from whole genome alignments of strains, and these are generally interpreted to reflect clonal relationships. Using new methods based on the statistics of single-nucleotide polymorphism (SNP) splits, we show that this interpretation is incorrect. For many species, each locus has recombined many times along its line of descent, and instead of many loci supporting a common phylogeny, the phylogeny changes many thousands of times along the genome alignment. Analysis of the patterns of allele sharing among strains shows that bacterial populations cannot be approximated as either clonal or freely recombining but are structured such that recombination rates between lineages vary over several orders of magnitude, with a unique pattern of rates for each lineage. Thus, rather than reflecting clonal ancestry, whole genome phylogenies reflect distributions of recombination rates.

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Christopher Field

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