Secretion and fusion of biogeochemically active archaeal membrane vesicles

Author:

Johnson Tyler B.1ORCID,Mach Collin1,Grove Ryan2,Kelly Robert3,Van Cott Kevin4,Blum Paul15

Affiliation:

1. Center for Genetics School of Biological Sciences University of Nebraska Lincoln Nebraska

2. Department of Biochemistry and the Redox Biology Center University of Nebraska‐Lincoln Lincoln Nebraska

3. Department of Chemical and Biomolecular Engineering North Carolina State University Raleigh North Carolina

4. Department of Chemical and Biomolecular Engineering University of Nebraska Lincoln Nebraska

5. Department of Microbiology and Environmental Toxicology University of California Santa Cruz California

Abstract

AbstractMicrobes belonging to the genus Metallosphaera oxidize sulfidic minerals. These organisms thrive at temperature extremes and are members of the archaeal phylum Crenarchaeota. Because they can employ a lithoautotrophic metabolism, energy availability likely limits their activity raising questions about how they conduct biogeochemical activity. Vesicles are membrane encapsulated structures produced by all biological lineages but using very different mechanisms. Across the Crenarchaeota, it has been proposed that a eukaryotic‐like Endosomal Sorting Complex Required for Transport system promotes formation of these structures but in response to unknown signals and for undefined purposes. To address such questions, Metallosphaera sedula vesicle formation and function were studied under lithoautotrophic conditions. Energy deprivation was evaluated and found to stimulate vesicle synthesis while energy excess repressed vesicle formation. Purified vesicles adhered rapidly to the primary copper ore, chalcopyrite, and formed compact monolayers. These vesicle monolayers catalyzed iron oxidation and solubilization of mineralized copper in a time‐dependent process. As these activities were membrane associated, their potential transfer by vesicle fusion to M. sedula cells was examined. Fluorophore‐loaded vesicles rapidly transferred fluorescence under environmentally relevant conditions. Vesicles from a related archaeal species were also capable of fusion; however, this process was species‐specific as vesicles from different species were incapable of fusion. In addition, vesicles produced by a copper‐resistant M. sedula cell line transferred copper extrusion capacity along with improved viability over mutant M. sedula cells lacking copper transport proteins. Membrane vesicles may therefore play a role in modulating energy‐related traits in geochemical environments by fusion‐mediated protein delivery.

Funder

Air Force Office of Scientific Research

Nebraska Center for Energy Sciences Research, University of Nebraska-Lincoln

Publisher

Wiley

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