Multicellular magnetotactic bacterial consortia are metabolically differentiated and not clonal

Schaible, G. A.; Jay, Z. J.; Cliff, J.; Schulz, F.; Gauvin, C.; Goudeau, D.; Malmstrom, R.; Ruff, S. E.; Edgcomb, V. P.; Hatzenpichler, R.

doi:10.1101/2023.11.27.568837

bioRxiv · 10.1101/2023.11.27.568837

Multicellular magnetotactic bacterial consortia are metabolically differentiated and not clonal

Schaible, G. A.·Jay, Z. J.·Cliff, J.·Schulz, F.·Gauvin, C.·Goudeau, D.·Malmstrom, R.·Ruff, S. E.·Edgcomb, V. P.·Hatzenpichler, R.

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Abstract

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 eight 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 nano-scale secondary ion mass spectrometry (NanoSIMS). By coupling FISH with bioorthogonal non-canonical 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. Significance statementThe emergence of multicellular lifeforms represents a pivotal milestone in Earths history, ushering in a new era of biological complexity. Because of the relative scarcity of multicellularity in the domains Bacteria and Archaea, research on the evolution of multicellularity has predominantly focused on eukaryotic model organisms. In this study, we explored the complexity of the only known bacteria without a unicellular stage in their life cycle, consortia of multicellular magnetotactic bacteria (MMB). Genomic and physiological analyses revealed that cells within individual MMB consortia are not clonal and exhibit metabolic differentiation. This implies a higher level of complexity than previously assumed for MMB consortia, prompting a reevaluation of the evolutionary factors that have led to the emergence of multicellularity. Because of their unique biology MMB consortia are ideally suited to become a model system to explore the underpinnings of bacterial multicellularity.

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Schaible, G. A., Jay, Z. J., Cliff, J., Schulz, F., Gauvin, C., Goudeau, D., Malmstrom, R., Ruff, S. E., Edgcomb, V. P., Hatzenpichler, R.. 2023-11-27. Multicellular magnetotactic bacterial consortia are metabolically differentiated and not clonal. https://doi.org/10.1101/2023.11.27.568837

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