Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses
Abstract
The extremely thermoacidophilic archaeon Metallosphaera sedula mobilizes metals by novel membrane-associated oxidase clusters and, consequently, requires metal resistance strategies. This issue was examined by “shocking” M. sedula with representative metals (Co 2+ , Cu 2+ , Ni 2+ , UO 2 2+ , Zn 2+ ) at inhibitory and subinhibitory levels. Collectively, one-quarter of the genome (554 open reading frames [ORFs]) responded to inhibitory levels, and two-thirds (354) of the ORFs were responsive to a single metal. Cu 2+ (259 ORFs, 106 Cu 2+ -specific ORFs) and Zn 2+ (262 ORFs, 131 Zn 2+ -specific ORFs) triggered the largest responses, followed by UO 2 2+ (187 ORFs, 91 UO 2 2+ -specific ORFs), Ni 2+ (93 ORFs, 25 Ni 2+ -specific ORFs), and Co 2+ (61 ORFs, 1 Co 2+ -specific ORF). While one-third of the metal-responsive ORFs are annotated as encoding hypothetical proteins, metal challenge also impacted ORFs responsible for identifiable processes related to the cell cycle, DNA repair, and oxidative stress. Surprisingly, there were only 30 ORFs that responded to at least four metals, and 10 of these responded to all five metals. This core transcriptome indicated induction of Fe-S cluster assembly (Msed_1656-Msed_1657), tungsten/molybdenum transport (Msed_1780-Msed_1781), and decreased central metabolism. Not surprisingly, a metal-translocating P-type ATPase (Msed_0490) associated with a copper resistance system (Cop) was upregulated in response to Cu 2+ (6-fold) but also in response to UO 2 2+ (4-fold) and Zn 2+ (9-fold). Cu 2+ challenge uniquely induced assimilatory sulfur metabolism for cysteine biosynthesis, suggesting a role for this amino acid in Cu 2+ resistance or issues in sulfur metabolism. The results indicate that M. sedula employs a range of physiological and biochemical responses to metal challenge, many of which are specific to a single metal and involve proteins with yet unassigned or definitive functions.
Document Details
- Document Type
- Pub Defense Publication
- Publication Date
- Aug 01, 2016
- Source ID
- 10.1128/aem.01176-16
Entities
People
- Arpan Mukherjee
- Garrett H. Wheaton
- Robert M. Kelly
Organizations
- Air Force Office of Scientific Research
- Defense Threat Reduction Agency
- North Carolina State University