| Full text | |
| Author(s): Show less - |
Lorenzetti, Alan P. R.
;
Kusebauch, Ulrike
;
Zaramela, Livia S.
;
Wu, Wei-Ju
;
de Almeida, Joao P. P.
;
Turkarslan, Serdar
;
L. G. de Lomana, Adrian
;
Gomes-Filho, Jose V.
;
Vencio, Ricardo Z. N.
;
Moritz, Robert L.
;
Koide, Tie
;
Baliga, Nitin S.
Total Authors: 12
|
| Document type: | Journal article |
| Source: | MSYSTEMS; v. 8, n. 2, p. 22-pg., 2023-03-13. |
| Abstract | |
The scale of post-transcriptional regulation and the implications of its interplay with other forms of regulation in environmental acclimation are underexplored for organisms of the domain Archaea. Here, we have investigated the scale of post-transcriptional regulation in the extremely halophilic archaeon Halobacterium salinarum NRC-1 by integrating the transcriptome-wide locations of transcript processing sites (TPSs) and SmAP1 binding, the genome-wide locations of antisense RNAs (asRNAs), and the consequences of RNase_2099C knockout on the differential expression of all genes. This integrated analysis has discovered that 54% of all protein-coding genes in the genome of this haloarchaeon are likely targeted by multiple mechanisms for putative post-transcriptional processing and regulation, with about 20% of genes likely being regulated by combinatorial schemes involving SmAP1, asRNAs, and RNase_2099C. Comparative analysis of mRNA levels (transcriptome sequencing [RNA-Seq]) and protein levels (sequential window acquisition of all theoretical fragment ion spectra mass spectrometry [SWATH-MS]) for 2,579 genes over four phases of batch culture growth in complex medium generated additional evidence for the conditional post-transcriptional regulation of 7% of all protein-coding genes. We demonstrate that post transcriptional regulation may act to fine-tune specialized and rapid acclimation to stressful environments, e.g., as a switch to turn on gas vesicle biogenesis to promote vertical relocation under anoxic conditions and modulate the frequency of transposition by insertion sequence (IS) elements of the IS200/IS605, IS4, and ISH3 families. Findings from this study are provided as an atlas in a public Web resource (https://halodata.systemsbiology.net).IMPORTANCE While the transcriptional regulation landscape of archaea has been extensively investigated, we currently have limited knowledge about post-transcriptional regulation and its driving mechanisms in this domain of life. In this study, we collected and integrated omics data from multiple sources and technologies to infer post -transcriptionally regulated genes and the putative mechanisms modulating their expression at the protein level in Halobacterium salinarum NRC-1. The results suggest that post-transcriptional regulation may drive environmental acclimation by regulating hallmark biological processes. To foster discoveries by other research groups interested in the topic, we extended our integrated data to the public in the form of an interactive atlas (https://halodata.systemsbiology.net). (AU) | |
| FAPESP's process: | 17/03052-2 - Non-coding RNAs derived from insertion sequences in the halophilic archaeon Halobacterium salinarum NRC-1 |
| Grantee: | Alan Péricles Rodrigues Lorenzetti |
| Support Opportunities: | Scholarships in Brazil - Doctorate |
| FAPESP's process: | 15/21038-1 - The antisense transcriptome of the halophilic archaeon Halobacterium salinarum |
| Grantee: | Tie Koide |
| Support Opportunities: | Regular Research Grants |
| FAPESP's process: | 11/07487-7 - Identification and characterization of Lsm-binding non-coding RNAs in the extremophile Halobacterium salinarum |
| Grantee: | Lívia Soares Zaramela |
| Support Opportunities: | Scholarships in Brazil - Doctorate |
| FAPESP's process: | 19/13440-5 - Detection of Insertion Sequence-encoded transposases using proteome data |
| Grantee: | Alan Péricles Rodrigues Lorenzetti |
| Support Opportunities: | Scholarships abroad - Research Internship - Doctorate |
| FAPESP's process: | 13/21522-5 - Functional characterization of non-coding RNAs associated with IS1341 transposons in Halobacterium salinarum |
| Grantee: | José Vicente Gomes Filho |
| Support Opportunities: | Scholarships in Brazil - Doctorate (Direct) |
| FAPESP's process: | 09/09532-0 - Systems biology of the extremophile Halobacterium salinarum: role of the non-coding RNAs in the global gene regulatory network model |
| Grantee: | Tie Koide |
| Support Opportunities: | Research Grants - Young Investigators Grants |