The Complex Transcriptional Landscape of Magnetosome Gene Clusters in Magnetospirillum gryphiswaldense

Dziuba, Marina; Riese, Cornelius N.; Borgert, Lion; Wittchen, Manuel; Busche, Tobias; Kalinowski, Jörn; Uebe, René; Schüler, Dirk

doi:10.1128/msystems.00893-21

Cited by 9 publications

(13 citation statements)

References 61 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This indicates the presence of an internal transcription start site (TSS) and its associated promoter within the coding sequence of mamO instead of the full transcription of the gene. Localization of an active promoter within mamO was recently described in MSR-1, suggesting that the transcriptional organization of MGCs may be more broadly conserved across MTB than assumed before 39 .…”

Section: Resultsmentioning

confidence: 88%

See 1 more Smart Citation

Hidden Talents: Silent Gene Clusters Encoding Magnetic Organelle Biosynthesis in a Non-Magnetotactic Phototrophic Bacterium

Dziuba

Paulus

Schramm

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

Magnetosomes are unique organelles synthesized by magnetotactic bacteria (MTB) for magnetic navigation. Their complex biosynthesis is controlled by large magnetosome gene clusters (MGC). Here, we report the discovery and comprehensive analysis of silent but functional MGCs in the non-magnetotactic phototrophic bacterium Rhodovastum atsumiense. Our findings suggest that these MGCs were acquired by horizontal gene transfer and inactivated through transcriptional silencing and antisense RNA regulation. At least several magnetosome genes from G2-11 retained functionality, as their products restore magnetosome biosynthesis in isogenic deletion mutants of the model MTB Magnetospirillum gryphiswaldense. Although G2-11 was found to form magnetosomes upon the laboratory transfer of the MGCs from M. gryphiswaldense, strong negative selection led to rapid loss of this trait upon subcultivation. Our results provide insight into the horizontal dissemination of gene clusters encoding bacterial magnetic organelles outside MTB and illuminate the potential mechanisms of their genomic preservation in a latent state.

show abstract

Section: Resultsmentioning

confidence: 88%

“…Localization of an active promoter within mamO was recently described in MSR-1, suggesting that the transcriptional organization of MGCs may be more broadly conserved across MTB than assumed before 39 .…”

Section: Rnaseq Reveals Poor Expression Levels and Antisense Transcri...mentioning

confidence: 88%

Hidden Talents: Silent Gene Clusters Encoding Magnetic Organelle Biosynthesis in a Non-Magnetotactic Phototrophic Bacterium

Dziuba

Paulus

Schramm

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In R. sphaeroides , the mic60□orf52 gene pair is co-transcribed as indicated by a transcription start site (TSS) in the intergenic region between hemD and mic60 (Myers et al 2020) (Fig 2A). In the magnetosome gene island (MAI) of Magnetospirillum gryphiswaldense, mic60 and orf52 are also co-transcribed separately from their neighboring genes (Dziuba et al 2021). The conserved motif order and composition, as well as transcriptional coupling, of Mic60 and Orf52 indicate that these proteins have structural roles and may physically interact with each other at alphaproteobacterial envelopes.…”

Section: Resultsmentioning

confidence: 99%

The development of intracytoplasmic membranes in alphaproteobacteria involves the conserved mitochondrial crista-developing protein Mic60

Muñoz-Gómez

Cadena

Gardiner

et al. 2022

Preprint

View full text Add to dashboard Cite

Mitochondrial cristae expand the surface area of respiratory membranes and ultimately allow for the evolutionary scaling of respiration with cell volume across eukaryotes. The discovery of Mic60 homologs among alphaproteobacteria, the closest extant relatives of mitochondria, suggested that cristae might have evolved from bacterial intracytoplasmic membranes (ICMs). Here, we investigated the predicted structure and function of alphaproteobacterial Mic60, and a protein encoded by an adjacent gene Orf52, in two distantly related purple alphaproteobacteria, Rhodobacter sphaeroides and Rhodopseudomonas palustris. In addition, we assessed the potential physical interactors of Mic60 and Orf52 in R. sphaeroides. We show that the three alpha-helices of mitochondrial Mic60's mitofilin domain, as well as its adjacent membrane-binding amphipathic helix, are present in alphaproteobacterial Mic60. The disruption of Mic60 and Orf52 caused photoheterotrophic growth defects, which are most severe under low light conditions, and both their disruption and overexpression lead to enlarged ICMs in both studied alphaproteobacteria. We also found that alphaproteobacterial Mic60 physically interacts with BamA, the homolog of Sam50, one of the main physical interactors of eukaryotic Mic60. This interaction, responsible for making contact sites at mitochondrial envelopes, has been conserved in modern alphaproteobacteria despite more than a billion years of evolutionary divergence. Our results suggest a role for Mic60 in photosynthetic ICM development and contact site formation at alphaproteobacterial envelopes. Overall, we provide support for the hypothesis that mitochondrial cristae evolved from alphaproteobacterial ICMs, and therefore have improved our understanding of the nature of the mitochondrial ancestor.

show abstract

“…Transfer of all five mam - and mms -operons (MagOPs) from M. gryphiswaldense , conferred magnetosome biosynthesis to various foreign, hitherto non-magnetic bacteria, thereby confirming the essential role of this gene set [ 16 , 17 ]. A recent analysis by RNA-sequencing, bioluminescence reporter assays and promoter knockouts revealed that the transcriptional architecture of magnetosome operons is complex [ 18 ]: in microaerobically grown cells, the mamGFDCop (2.1 kb) and feoAB1op (2.4 kb) operons are transcribed as single transcriptional units, whereas multiple transcription start sites (TSS) were present in the mms6op (3.6 kb), mamXYop (5 kb) and the long mamABop (> 16 kb), which comprises 17 genes and encodes all the essential factors for magnetosome biosynthesis [ 13 , 19 ].…”

Section: Introductionmentioning

confidence: 99%

“…However, although these previous studies already revealed valuable insights into the transcriptional organization and the role of oxygen, major parts of the regulation and transcriptional architecture are still unknown. Most importantly, previous studies [ 18 , 28 ] employed microoxic conditions supporting fastest growth, but suboptimal magnetosome formation, as indicated by the formation of fewer, less regular and smaller magnetosomes compared to anoxic conditions [ 25 , 26 ]. Furthermore, the operon architecture and transcriptional organization of genes involved in magnetosome biosynthesis outside the MAI has remained unknown.…”

Section: Introductionmentioning

confidence: 99%

The transcriptomic landscape of Magnetospirillum gryphiswaldense during magnetosome biomineralization

et al. 2022

Self Cite

View full text Add to dashboard Cite

Background One of the most complex prokaryotic organelles are magnetosomes, which are formed by magnetotactic bacteria as sensors for navigation in the Earth’s magnetic field. In the alphaproteobacterium Magnetospirillum gryphiswaldense magnetosomes consist of chains of magnetite crystals (Fe3O4) that under microoxic to anoxic conditions are biomineralized within membrane vesicles. To form such an intricate structure, the transcription of > 30 specific structural genes clustered within the genomic magnetosome island (MAI) has to be coordinated with the expression of an as-yet unknown number of auxiliary genes encoding several generic metabolic functions. However, their global regulation and transcriptional organization in response to anoxic conditions most favorable for magnetite biomineralization are still unclear. Results Here, we compared transcriptional profiles of anaerobically grown magnetosome forming cells with those in which magnetosome biosynthesis has been suppressed by aerobic condition. Using whole transcriptome shotgun sequencing, we found that transcription of about 300 of the > 4300 genes was significantly enhanced during magnetosome formation. About 40 of the top upregulated genes are directly or indirectly linked to aerobic and anaerobic respiration (denitrification) or unknown functions. The mam and mms gene clusters, specifically controlling magnetosome biosynthesis, were highly transcribed, but constitutively expressed irrespective of the growth condition. By Cappable-sequencing, we show that the transcriptional complexity of both the MAI and the entire genome decreased under anaerobic conditions optimal for magnetosome formation. In addition, predominant promoter structures were highly similar to sigma factor σ70 dependent promoters in other Alphaproteobacteria. Conclusions Our transcriptome-wide analysis revealed that magnetite biomineralization relies on a complex interplay between generic metabolic processes such as aerobic and anaerobic respiration, cellular redox control, and the biosynthesis of specific magnetosome structures. In addition, we provide insights into global regulatory features that have remained uncharacterized in the widely studied model organism M. gryphiswaldense, including a comprehensive dataset of newly annotated transcription start sites and genome-wide operon detection as a community resource (GEO Series accession number GSE197098).

show abstract

The Complex Transcriptional Landscape of Magnetosome Gene Clusters in Magnetospirillum gryphiswaldense

Cited by 9 publications

References 61 publications

Hidden Talents: Silent Gene Clusters Encoding Magnetic Organelle Biosynthesis in a Non-Magnetotactic Phototrophic Bacterium

Hidden Talents: Silent Gene Clusters Encoding Magnetic Organelle Biosynthesis in a Non-Magnetotactic Phototrophic Bacterium

The development of intracytoplasmic membranes in alphaproteobacteria involves the conserved mitochondrial crista-developing protein Mic60

The transcriptomic landscape of Magnetospirillum gryphiswaldense during magnetosome biomineralization

Contact Info

Product

Resources

About