Multicellular magnetotactic bacteria are genetically heterogeneous consortia with metabolically differentiated cells

Schaible, George A.; Jay, Zackary J.; Cliff, John; Schulz, Frederik; Gauvin, Colin; Goudeau, Danielle; Malmstrom, Rex R.; Ruff, S. Emil; Edgcomb, Virginia; Hatzenpichler, Roland; Shou, ed., Wenying

doi:10.1371/journal.pbio.3002638

Title: Multicellular magnetotactic bacteria are genetically heterogeneous consortia with metabolically differentiated cells

Journal Article · Thu Jul 11 00:00:00 UTC 2024 · PLoS Biology (Online)

DOI: https://doi.org/10.1371/journal.pbio.3002638 · OSTI ID:2397021

Schaible, George A.; Jay, Zackary J.; Cliff, John; Schulz, Frederik; Gauvin, Colin; Goudeau, Danielle; Malmstrom, Rex R.; Ruff, S. Emil; Edgcomb, Virginia;

; Shou, ed., Wenying

Consortia of multicellular magnetotactic bacteria (MMB) are currently the only known example of bacteria without a unicellular stage in their life cycle. Because of their recalcitrance to cultivation, most previous studies of MMB have been limited to microscopic observations. To study the biology of these unique organisms in more detail, we use multiple culture-independent approaches to analyze the genomics and physiology of MMB consortia at single-cell resolution. We separately sequenced the metagenomes of 22 individual MMB consortia, representing 8 new species, and quantified the genetic diversity within each MMB consortium. This revealed that, counter to conventional views, cells within MMB consortia are not clonal. Single consortia metagenomes were then used to reconstruct the species-specific metabolic potential and infer the physiological capabilities of MMB. To validate genomic predictions, we performed stable isotope probing (SIP) experiments and interrogated MMB consortia using fluorescence in situ hybridization (FISH) combined with nanoscale secondary ion mass spectrometry (NanoSIMS). By coupling FISH with bioorthogonal noncanonical amino acid tagging (BONCAT), we explored their in situ activity as well as variation of protein synthesis within cells. We demonstrate that MMB consortia are mixotrophic sulfate reducers and that they exhibit metabolic differentiation between individual cells, suggesting that MMB consortia are more complex than previously thought. These findings expand our understanding of MMB diversity, ecology, genomics, and physiology, as well as offer insights into the mechanisms underpinning the multicellular nature of their unique lifestyle.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: Environmental Molecular Sciences Laboratory (EMSL); USDOE; USDOE Joint Genome Institute (JGI); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725; AC05-76RL01830

OSTI ID:: 2397021

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Journal Issue: 7 Vol. 22; ISSN 1545-7885

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
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Title: Multicellular magnetotactic bacteria are genetically heterogeneous consortia with metabolically differentiated cells

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