Photoglobin, a distinct family of non-heme binding globins, defines a potential photosensor in prokaryotic signal transduction systems

Schneider, Theresa; Tan, Yan‐Xi; Li, Huan; Fisher, Jonathan S.; Zhang, David

doi:10.1016/j.csbj.2021.12.022

Cited by 13 publications

(7 citation statements)

References 103 publications

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“…Given the general association of these globins with candidate HO and FDBR proteins, we designate them as bilin biosynthesis-associated globins (BBAGs) and number them based on the type of pre-PcyA with which they are associated. For phylogenetic analysis of BBAGs, we also included phycobiliproteins and globin–B12 fusion proteins recently designated as photoglobins ( 60 ). Homology to photoglobins allowed us to use the RsbR globin domain ( 61 ) as an outgroup.…”

Section: Resultsmentioning

confidence: 99%

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Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Rockwell

Martin

Lagarias

2023

Proc. Natl. Acad. Sci. U.S.A.

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Terrestrial ecosystems and human societies depend on oxygenic photosynthesis, which began to reshape our atmosphere approximately 2.5 billion years ago. The earliest known organisms carrying out oxygenic photosynthesis are the cyanobacteria, which use large complexes of phycobiliproteins as light-harvesting antennae. Phycobiliproteins rely on phycocyanobilin (PCB), a linear tetrapyrrole (bilin) chromophore, as the light-harvesting pigment that transfers absorbed light energy from phycobilisomes to the chlorophyll-based photosynthetic apparatus. Cyanobacteria synthesize PCB from heme in two steps: A heme oxygenase converts heme into biliverdin IXα (BV), and the ferredoxin-dependent bilin reductase (FDBR) PcyA then converts BV into PCB. In the current work, we examine the origins of this pathway. We demonstrate that PcyA evolved from pre-PcyA proteins found in nonphotosynthetic bacteria and that pre-PcyA enzymes are active FDBRs that do not yield PCB. Pre-PcyA genes are associated with two gene clusters. Both clusters encode bilin-binding globin proteins, phycobiliprotein paralogs that we designate as BBAGs (bilin biosynthesis-associated globins). Some cyanobacteria also contain one such gene cluster, including a BBAG, two V4R proteins, and an iron–sulfur protein. Phylogenetic analysis shows that this cluster is descended from those associated with pre-PcyA proteins and that light-harvesting phycobiliproteins are also descended from BBAGs found in other bacteria. We propose that PcyA and phycobiliproteins originated in heterotrophic, nonphotosynthetic bacteria and were subsequently acquired by cyanobacteria.

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Section: Resultsmentioning

confidence: 99%

“…5 B ). The BBAG-2 lineage also includes photoglobins ( 60 ) and globins associated with the atypical pre-1 sequences NJL04020 and NJO05336 ( Fig. 3 B ).…”

Section: Resultsmentioning

confidence: 99%

Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Rockwell

Martin

Lagarias

2023

Proc. Natl. Acad. Sci. U.S.A.

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“…This has served as a foundation for homologous sequence searches, structural similarity searches, and phylogenetic analysis. Developments of bioinformatics methods, including sequence similarity based (i.e., BLAST), sequence–profile comparison based (i.e., PSIBLAST, HMMER), profile–profile comparison based (HHsearch), and structural similarity based (i.e., Dali), have led to the identification and unification of many protein sequences into families, families into superfamilies, and superfamilies into common folds (Andreeva et al, 2004; Aravind & Koonin, 2001; Cheng et al, 2014; Schneider et al, 2022; Tan et al, 2021; Zhang & Aravind, 2010; Zhang, Iyer, et al, 2012). One of our contributions in this regard is the identification of a shared structural core, the BECR fold, among many metal‐independent RNases (Zhang, de Souza, et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Ribonuclease T2 represents a distinct circularly permutated version of the BECR RNases

Schneider

Tan

et al. 2022

Protein Science

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Detection of homologous relationships among proteins and understanding their mechanisms of diversification are major topics in the fields of protein science, bioinformatics, and phylogenetics. Recent developments in sequence/ profile-based and structural similarity-based methods have greatly facilitated the unification and classification of many protein families into superfamilies or folds, yet many proteins remain unclassified in current protein databases.As one of the three earliest identified RNases in biology, ribonuclease T2, also known as RNase I in Escherichia coli, RNase Rh in fungi, or S-RNase in plant, is thought to be an ancient RNase family due to its widespread distribution and distinct structure. In this study, we present evidence that RNase T2 represents a circularly permutated version of the BECR (Barnase-EndoU-Colicin E5/D-RelE) fold RNases. This subtle relationship cannot be detected by traditional methods such as sequence/profile-based comparisons, structuresimilarity searches, and circular permutation detections. However, we were able to identify the structural similarity using rational reconstruction of a theoretical RNase T2 ancestor via a reverse circular permutation process, followed by structural modeling using AlphaFold2, and structural comparisons. This relationship is further supported by the fact that RNase T2 and other typical BECR RNases, namely Colicin D, RNase A, and BrnT, share similar catalytic site configurations, all involving an analogous set of conserved residues on the α0 helix and the β4 strand of the BECR fold. This study revealed a hidden root of RNase T2 in bacterial toxin systems and demonstrated that reconstruction and modeling of ancestral topology is an effective strategy to identify remote relationship between proteins.

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“…On exposure to light, B 12 photochemistry triggers structural changes culminating in the dissociation of the tetramer, concomitant release from DNA and ultimately transcription initiation. More complex putative B 12 photoreceptors have since been identi ed in genomes, but lack functional characterisation 4,5 . Sequence analysis reveals many CarH-like homologues form considerably more complex protein architectures, with the B 12 -binding domain fused to additional enzyme or chromophore-binding domains 4 .…”

Section: Introductionmentioning

confidence: 99%

“…Sequence analysis reveals many CarH-like homologues form considerably more complex protein architectures, with the B 12 -binding domain fused to additional enzyme or chromophore-binding domains 4 . Here we describe a new subfamily of B 12 -dependent photoreceptors, consisting of a B 12 binding domain fused to a globin-like (or photoglobin 5 ) domain. The hypothesis that these coupled photoglobin and B 12 -binding domains may act as a light-sensing regulatory bundle 5 provides exciting opportunities to develop new optogenetic tools.…”

Section: Introductionmentioning

confidence: 99%

Photocobilins integrate B12 and bilin photochemistry for enzyme control

Scrutton

Zhang

Poddar

et al. 2023

Preprint

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Photoreceptor proteins utilise chromophores to sense light and trigger a biological response. The discovery that cobalamin (vitamin B12) can act as a light-sensing chromophore heralded a new field of B12-photobiology. Although microbial genome analysis indicates that photoactive B12-binding domains form part of more complex protein architectures, regulating a range of molecular–cellular functions in response to light, experimental evidence is lacking. Here we identify and characterise a sub-family of multi-centre photoreceptors, termed photocobilins, that use B12 and biliverdin (BV) to sense light across the visible spectrum. Crystal structures reveal close juxtaposition of the B12 and BV chromophores, an arrangement that facilitates optical coupling. Light-triggered conversion of the B12 affects quaternary structure, in turn leading to light-activation of associated enzyme domains. The apparent widespread nature of photocobilins implies involvement in light regulation of a wider array of biochemical processes, and thus expand the scope for B12 photobiology. Their characterisation provides inspiration for the design of broad-spectrum optogenetic tools and next generation bio-photocatalysts.

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Photoglobin, a distinct family of non-heme binding globins, defines a potential photosensor in prokaryotic signal transduction systems

Abstract: Graphical abstract

Cited by 13 publications

References 103 publications

Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Ribonuclease T2 represents a distinct circularly permutated version of the BECR RNases

Photocobilins integrate B12 and bilin photochemistry for enzyme control

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