B.Sc. Biology, Ludwig Maximilian University (LMU), Munich/Germany (2013)
M.Sc. Biology and bioimaging, Ludwig Maximilian University (LMU), Munich/Germany (2015)
Ph.D., Animal-Microbe Symbioses, Max Planck Institute for Marine Microbiology in Bremen/Germany (2020)
Benedikt joined the Amieva Lab from Germany in 2022. During his B.Sc. and M.Sc. programs in zoology, he became fascinated with 3D imaging approaches to study small animal microanatomy. He spent his PhD developing in situ imaging approaches to study deep-sea symbioses and fell in love with studying host-microbe interactions. In the Amieva Lab, Benedikt will advance his previously developed correlative chemical imaging techniques to resolve metabolic and cellular interactions that drive H. pylori pathogenesis in the gastric glands.
Honors & Awards
Newcomb Cleveland Prize for most outstanding scientific paper of 2022 (coauthor), American Association for the Advancement of Science (2022)
Postdoctoral fellowship, Human Frontier in Science Program (HFSP) long-term fellowship (2022)
Best talk during “IT MA(t)TERs Conference”, Max Planck Institutes for Terrestrial and Marine Microbiology (2021)
Otto Hahn Medal for outstanding scientific achievements during doctorate studies, Max Planck Society (2021)
Best students’ poster of the International Max Planck Research Schools program Marmic, Max Planck Institute for Marine Microbiology (2019)
Best students’ talk at the annual ISCE conference, International Society of Chemical Ecology (ISCE) (2019)
MDPI 2018 travel award, Metabolites (2018)
MSI Award for “brilliant ideas or works achieved using mass spectrometry imaging techniques”, ImaBiotech (2018)
Manuel Amieva, Postdoctoral Faculty Sponsor
Connecting structure and function from organisms to molecules in small-animal symbioses through chemo-histo-tomography
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2021; 118 (27)
Our understanding of metabolic interactions between small symbiotic animals and bacteria or parasitic eukaryotes that reside within their bodies is extremely limited. This gap in knowledge originates from a methodological challenge, namely to connect histological changes in host tissues induced by beneficial and parasitic (micro)organisms to the underlying metabolites. We addressed this challenge and developed chemo-histo-tomography (CHEMHIST), a culture-independent approach to connect anatomic structure and metabolic function in millimeter-sized symbiotic animals. CHEMHIST combines chemical imaging of metabolites based on mass spectrometry imaging (MSI) and microanatomy-based micro-computed X-ray tomography (micro-CT) on the same animal. Both high-resolution MSI and micro-CT allowed us to correlate the distribution of metabolites to the same animal's three-dimensional (3D) histology down to submicrometer resolutions. Our protocol is compatible with tissue-specific DNA sequencing and fluorescence in situ hybridization for the taxonomic identification and localization of the associated micro(organisms). Building CHEMHIST upon in situ imaging, 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. Combining MSI and micro-CT, we present a methodological groundwork for connecting metabolic and anatomic phenotypes of small symbiotic animals that often represent keystone species for ecosystem functioning.
View details for DOI 10.1073/pnas.2023773118
View details for Web of Science ID 000685026600003
View details for PubMedID 34183413
View details for PubMedCentralID PMC8300811
Hunting the eagle killer: A cyanobacterial neurotoxin causes vacuolar myelinopathy
2021; 371 (6536): 1335-+
Vacuolar myelinopathy is a fatal neurological disease that was initially discovered during a mysterious mass mortality of bald eagles in Arkansas in the United States. The cause of this wildlife disease has eluded scientists for decades while its occurrence has continued to spread throughout freshwater reservoirs in the southeastern United States. Recent studies have demonstrated that vacuolar myelinopathy is induced by consumption of the epiphytic cyanobacterial species Aetokthonos hydrillicola growing on aquatic vegetation, primarily the invasive Hydrilla verticillata Here, we describe the identification, biosynthetic gene cluster, and biological activity of aetokthonotoxin, a pentabrominated biindole alkaloid that is produced by the cyanobacterium A. hydrillicola We identify this cyanobacterial neurotoxin as the causal agent of vacuolar myelinopathy and discuss environmental factors-especially bromide availability-that promote toxin production.
View details for DOI 10.1126/science.aax9050
View details for Web of Science ID 000636043400031
View details for PubMedID 33766860
View details for PubMedCentralID PMC8318203
Spatial metabolomics of in situ host-microbe interactions at the micrometre scale
2020; 5 (3): 498-+
Spatial metabolomics describes the location and chemistry of small molecules involved in metabolic phenotypes, defence molecules and chemical interactions in natural communities. Most current techniques are unable to spatially link the genotype and metabolic phenotype of microorganisms in situ at a scale relevant to microbial interactions. Here, we present a spatial metabolomics pipeline (metaFISH) that combines fluorescence in situ hybridization (FISH) microscopy and high-resolution atmospheric-pressure matrix-assisted laser desorption/ionization mass spectrometry to image host-microbe symbioses and their metabolic interactions. The metaFISH pipeline aligns and integrates metabolite and fluorescent images at the micrometre scale to provide a spatial assignment of host and symbiont metabolites on the same tissue section. To illustrate the advantages of metaFISH, we mapped the spatial metabolome of a deep-sea mussel and its intracellular symbiotic bacteria at the scale of individual epithelial host cells. Our analytical pipeline revealed metabolic adaptations of the epithelial cells to the intracellular symbionts and variation in metabolic phenotypes within a single symbiont 16S rRNA phylotype, and enabled the discovery of specialized metabolites from the host-microbe interface. metaFISH provides a culture-independent approach to link metabolic phenotypes to community members in situ and is a powerful tool for microbiologists across fields.
View details for DOI 10.1038/s41564-019-0664-6
View details for Web of Science ID 000510823400002
View details for PubMedID 32015496
Multiplexed neuropeptide mapping in ant brains integrating microtomography and three-dimensional mass spectrometry imaging.
2023; 2 (5): pgad144
Neuropeptides are important regulators of animal physiology and behavior. Hitherto the gold standard for the localization of neuropeptides have been immunohistochemical methods that require the synthesis of antibody panels, while another limiting factor has been the brain's opacity for subsequent in situ light or fluorescence microscopy. To address these limitations, we explored the integration of high-resolution mass spectrometry imaging (MSI) with microtomography for a multiplexed mapping of neuropeptides in two evolutionary distant ant species, Atta sexdens and Lasius niger. For analyzing the spatial distribution of chemically diverse peptide molecules across the brain in each species, the acquisition of serial mass spectrometry images was essential. As a result, we have comparatively mapped the three-dimensional (3D) distributions of eight conserved neuropeptides throughout the brain microanatomy. We demonstrate that integrating the 3D MSI data into high-resolution anatomy models can be critical for studying organs with high plasticity such as brains of social insects. Several peptides, like the tachykinin-related peptides (TK) 1 and 4, were widely distributed in many brain areas of both ant species, whereas others, for instance myosuppressin, were restricted to specific regions only. Also, we detected differences at the species level; many peptides were identified in the optic lobe of L. niger, but only one peptide (ITG-like) was found in this region in A. sexdens. Building upon MS imaging studies on neuropeptides in invertebrate model systems, our approach leverages correlative MSI and computed microtomography for investigating fundamental neurobiological processes by visualizing the unbiased 3D neurochemistry in its complex anatomic environment.
View details for DOI 10.1093/pnasnexus/pgad144
View details for PubMedID 37215633
Coming together-symbiont acquisition and early development in deep-sea bathymodioline mussels
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2021; 288 (1957): 20211044
How and when symbionts are acquired by their animal hosts has a profound impact on the ecology and evolution of the symbiosis. Understanding symbiont acquisition is particularly challenging in deep-sea organisms because early life stages are so rarely found. Here, we collected early developmental stages of three deep-sea bathymodioline species from different habitats to identify when these acquire their symbionts and how their body plan adapts to a symbiotic lifestyle. These mussels gain their nutrition from chemosynthetic bacteria, allowing them to thrive at deep-sea vents and seeps worldwide. Correlative imaging analyses using synchrotron-radiation based microtomography together with light, fluorescence and electron microscopy revealed that the pediveliger larvae were aposymbiotic. Symbiont colonization began during metamorphosis from a planktonic to a benthic lifestyle, with the symbionts rapidly colonizing first the gills, the symbiotic organ of adults, followed by all other epithelia of their hosts. Once symbiont densities in plantigrades reached those of adults, the host's intestine changed from the looped anatomy typical for bivalves to a straightened form. Within the Mytilidae, this morphological change appears to be specific to Bathymodiolus and Gigantidas, and is probably linked to the decrease in the importance of filter feeding when these mussels switch to gaining their nutrition largely from their symbionts.
View details for DOI 10.1098/rspb.2021.1044
View details for Web of Science ID 000687673400008
View details for PubMedID 34403628
View details for PubMedCentralID PMC8370805
Determination of Abundant Metabolite Matrix Adducts Illuminates the Dark Metabolome of MALDI-Mass Spectrometry Imaging Datasets
2021; 93 (24): 8399-8407
Spatial metabolomics using mass spectrometry imaging (MSI) is a powerful tool to map hundreds to thousands of metabolites in biological systems. One major challenge in MSI is the annotation of m/z values, which is substantially complicated by background ions introduced throughout the chemicals and equipment used during experimental procedures. Among many factors, the formation of adducts with sodium or potassium ions, or in case of matrix-assisted laser desorption ionization (MALDI)-MSI, the presence of abundant matrix clusters strongly increases total m/z peak counts. Currently, there is a limitation to identify the chemistry of the many unknown peaks to interpret their biological function. We took advantage of the co-localization of adducts with their parent ions and the accuracy of high mass resolution to estimate adduct abundance in 20 datasets from different vendors of mass spectrometers. Metabolites ranging from lipids to amines and amino acids form matrix adducts with the commonly used 2,5-dihydroxybenzoic acid (DHB) matrix like [M + (DHB-H2O) + H]+ and [M + DHB + Na]+. Current data analyses neglect those matrix adducts and overestimate total metabolite numbers, thereby expanding the number of unidentified peaks. Our study demonstrates that MALDI-MSI data are strongly influenced by adduct formation across different sample types and vendor platforms and reveals a major influence of so far unrecognized metabolite-matrix adducts on total peak counts (up to one third). We developed a software package, mass2adduct, for the community for an automated putative assignment and quantification of metabolite-matrix adducts enabling users to ultimately focus on the biologically relevant portion of the MSI data.
View details for DOI 10.1021/acs.analchem.0c04720
View details for Web of Science ID 000665642500005
View details for PubMedID 34097397
View details for PubMedCentralID PMC8223199
Armored with skin and bone: A combined histological and mu CT-study of the exceptional integument of the Antsingy leaf chameleon Brookesia perarmata (Angel, 1933)
JOURNAL OF MORPHOLOGY
2020; 281 (7): 754-764
Madagascar's endemic ground-dwelling leaf chameleons (Brookesiinae: Brookesia Gray, 1865 + Palleon Glaw, et al., Salamandra, 2013, 49, pp. 237-238) form the sister taxon to all other chameleons (i.e., the Chamaeleoninae). They possess a limited ability of color change, a rather dull coloration, and a nonprehensile tail assisting locomotion in the leaf litter on the forest floor. Most Brookesia species can readily be recognized by peculiar spiky dorsolateral projections ("Rückensäge"), which are caused by an aberrant vertebral structure and might function as body armor to prevent predation. In addition to a pronounced Rückensäge, the Antsingy leaf chameleon Brookesia perarmata (Angel, 1933) exhibits conspicuous, acuminate tubercle scales on the lateral flanks and extremities, thereby considerably enhancing the overall armored appearance. Such structures are exceptional within the Chamaeleonidae and despite an appreciable interest in the integument of chameleons in general, the morphology of these integumentary elements remains shrouded in mystery. Using various conventional and petrographic histological approaches combined with μCT-imaging, we reveal that the tubercle scales consist of osseous, multicusped cores that are embedded within the dermis. Based on this, they consequently can be interpreted as osteoderms, which to the best of our knowledge is the first record of such for the entire Chamaeleonidae and only the second one for the entire clade Iguania. The combination of certain aspects of tissue composition (especially the presence of large, interconnected, and marrow-filled cavities) together with the precise location within the dermis (being completely enveloped by the stratum superficiale), however, discriminate the osteoderms of B. perarmata from those known for all other lepidosaurs.
View details for DOI 10.1002/jmor.21135
View details for Web of Science ID 000533682900001
View details for PubMedID 32427377
Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra.
2016; 2: 16182
The reproduction mode of uncultivable microorganisms deserves investigation as it can largely diverge from conventional transverse binary fission. Here, we show that the rod-shaped gammaproteobacterium thriving on the surface of the Robbea hypermnestra nematode divides by FtsZ-based, non-synchronous invagination of its poles-that is, the host-attached and fimbriae-rich pole invaginates earlier than the distal one. We conclude that, in a naturally occurring animal symbiont, binary fission is host-oriented and does not require native FtsZ to polymerize into a ring at any septation stage.
View details for DOI 10.1038/nmicrobiol.2016.182
View details for PubMedID 27723729
A specific and widespread association between deep-sea Bathymodiolus mussels and a novel family of Epsilonproteobacteria
ENVIRONMENTAL MICROBIOLOGY REPORTS
2016; 8 (5): 805-813
Bathymodiolus mussels dominate animal communities at many hydrothermal vents and cold seeps. Essential to the mussels' ecological and evolutionary success is their association with symbiotic methane- and sulfur-oxidizing gammaproteobacteria, which provide them with nutrition. In addition to these well-known gammaproteobacterial endosymbionts, we found epsilonproteobacterial sequences in metatranscriptomes, metagenomes and 16S rRNA clone libraries as well as by polymerase chain reaction screening of Bathymodiolus species sampled from vents and seeps around the world. These epsilonproteobacterial sequences were closely related, indicating that the association is highly specific. The Bathymodiolus-associated epsilonproteobacterial 16S rRNA sequences were at most 87.6% identical to the closest cultured relative, and 91.2% identical to the closest sequences in public databases. This clade therefore represents a novel family within the Epsilonproteobacteria. Fluorescence in situ hybridization and transmission electron microscopy showed that the bacteria are filamentous epibionts associated with the gill epithelia in two Bathymodiolus species. In animals that host highly specific symbioses with one or a few types of endosymbionts, other less-abundant members of the microbiota can be easily overlooked. Our work highlights how widespread and specific associations with less-abundant microbes can be. Possibly, these microbes play an important role in the survival and health of their animal hosts.
View details for DOI 10.1111/1758-2229.12442
View details for Web of Science ID 000395002300035
View details for PubMedID 27428292