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Sequences, Domain Architectures, and Biological Functions of the Serine/Threonine and Histidine Kinases in Synechocystis sp. PCC 6803

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Abstract

The cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis) is a photoautotrophic prokaryote with plant-like photosynthetic machineries which significantly contribute to global carbon fixation and atmospheric oxygen production. Because of the relatively short cell doubling time, small size of the genome, and the ease for genetic manipulation, Synechocystis is a popular model organism for studies including photosynthesis and biofuel production. The cyanobacterium contains 12 eukaryotic type Ser/Thr kinases (SpkA–L) and 49 histidine kinases (Hik1–47 and Sll1334 and Sll5060 are named as Hik48 and Hik49, respectively, in this review) of the two-component system. All SpkA–L kinases have a eukaryotic kinase DFG signature in their A-loops. Based on the types of the kinase domains, the Spks can be separated into three groups: one group contains SpkA and SpkG which are related to human kinases, while SpkH–L are in another group that is distinct from human kinases. The third group contains SpkB–F which are between the first two groups. Four histidine kinases (Hiks17, 36, 45, and 48) lack a clear histidine kinase domain, and the conserved phosphorylatable histidine residue could not be identified for six histidine kinases (Hiks11, 18, 29, 37, 39, and 43) even though they have clear histidine kinase domains. Each of the remaining 39 has a histidine kinase domain with the conserved histidine residue. Eight hybrid histidine kinases contain one or two receiver domains, and they all, except Hik25 (Slr0222), have the conserved phosphorylatable aspartate. The disruptants of all kinases except hik13 and hik15 have been generated, and the majority of them have modest or no obvious phenotypes, indicating other kinases could functionally compensate the loss of a particular kinase. This review presents a comprehensive discussion including a spectrum of sequence, domain architecture, in vivo function, and proteomics investigations of Ser/Thr and histidine kinases. Understanding the sequences, domain architectures, and biology of the kinases will help to integrate “omic” data to clarify their exact biochemical functions.

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Acknowledgements

We thank Drs. Taylor and Perkins from the Department of Chemistry at the University of Louisiana at Lafayette and Jianping Yu from National Renewable Energy Laboratory for carefully reading and editing the manuscript.

Funding

The authors thank the support (NSF(2010)-PFUND-217 and LEQSF(2013-16)-RD-A-15) from the US National Science Foundation’s EPSCoR Program and Louisiana RCS Program to W.X.

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  1. Department of Chemistry, University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Wu Xu

  2. State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, No.1 West Beichen Rd., Beijing, 100101, China

    Yingchun Wang

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Electronic Supplementary Material

Supplementary Figure 1

Bacterial two-component systems. a, A typical His-Asp two-component system including a sensor & histidine kinase and a response regulator; b, A His-Asp-His-Asp phosphorelay including a hybrid histidine, a linker often with a Hpt domain and a response regulator. (PDF 25 kb)

Supplementary Figure 2

Domain architectures of the sensor and histidine kinases of Synechocystis without GAF and PAS domains. (PDF 41 kb)

Supplementary Figure 3

Domain architectures of the sensor and histidine kinases of Synechocystis with GAF domain(s). (PDF 22 kb)

Supplementary Figure 4

Domain architectures of the sensor and histidine kinases of Synechocystis with PAS domain(s). (PDF 22 kb)

Supplementary Figure 5

Domain architectures of the sensor and histidine kinases of Synechocystis with GAF and PAS domains. (PDF 22 kb)

Supplementary Figure 6

Domain architectures of the hybrid histidine kinases of Synechocystis with only one receiver domain. (PDF 45 kb)

Supplementary Figure 7

Domain architectures of the hybrid histidine kinases of Synechocystis with two receiver domains. (PDF 26 kb)

Supplementary Figure 8

A local 3-D structure shows hydrogen bond interactions between the conserved phosphorylatable His260 and its surrounding residues of a histidine kinase in PDB (PDB ID: 3DGE Chain A). His 260 participates in two hydrogen bonds: a hydrogen bond between His260:N and Ala256:O and the distance is 2.99 Å, and a hydrogen bond between His260:O and Glu261:N and the distance is 2.24 Å. Asn257 forms two hydrogen bonds to bridge Ala256 and Glu261 together: a hydrogen bond between Asn257:N and Ala256:O and the distance is 2.24 Å, and a hydrogen bond between Asn257:O and Glu261:N and the distance is 2.80 Å. (PDF 65 kb)

Supplementary Figure 9

Amino acid sequence alignments of the histidine kinases of Synechocystis with either similar sizes or domain architectures. a, A sequence alignment of the histidine kinases with similar sizes (650aa-1000aa) along with a histidine kinase in PDB (PDB ID: 3DGE Chain A). The conserved phosphorylatable histidine is labelled; b, A sequence alignments of the histidine kinases with similar domain architectures. Two conserved histidine residues are labelled; c, A sequence alignments of the histidine kinases with similar domain architectures. A conserved histidine residue is labelled. (PDF 86 kb)

Supplementary Figure 10

An amino acid sequence alignment of the histidine-containing phosphotransfer (Hpt) domains of Synechocystis histidine kinases along with two PAS domains (PDB IDs: 3MYF Chain A and 3US6 Chain A) from PDB. The conserved phosphorylatable histidine is labelled. (PDF 37 kb)

Supplementary Figure 11

An amino acid sequence alignment of the PAS domains of Synechocystis histidine kinases along with one PAS domain (PDB ID: 2VLG Chain A) from PDB. (PDF 76 kb)

Supplementary Figure 12

An amino acid sequence alignment of the PAS domains of Synechocystis histidine kinases with two or more PAS domains. A conserved Asp residue is labelled. (PDF 60 kb)

Supplementary Figure 13

An amino acid sequence alignment of the GAF domains of Synechocystis histidine kinases along with two GAF domains (PDB IDs: 2K2N Chain A and 2KOI Chain A) from PDB. (PDF 73 kb)

Supplementary Figure 14

An amino acid sequence alignment of the selected GAF domains of Synechocystis histidine kinases. a, The GAF domain of Hik35 is highly related to two GAF domains (PDB IDs: 2K2N Chain A and 2KOI Chain A) from PDB; b, An example of highly related GAF domains. (PDF 36 kb)

Supplementary Figure 15

An amino acid sequence alignment of PKN2 type of Ser/Thr kinases of Synechocystis. The DFG motif is labelled. (PDF 95 kb)

Supplementary Figure 16

An amino acid sequence alignment of ABC1 type of Ser/Thr kinases of Synechocystis. The DFG motif is labelled. (PDF 822 kb)

Supplementary Figure 17

Domain architecture of PKN2 type of Ser/Thr kinases of Synechocystis. (PDF 22 kb)

Supplementary Figure 18

Domain architecture of ABC1 type of Ser/Thr kinases of Synechocystis. (PDF 18 kb)

Supplementary Figure 19

An amino acid sequence alignment of Hik31 (chromosomal gene product) and Hik47 (plasmid gene product) of Synechocystis. (PDF 30 kb)

Supplementary Figure 20

Domain architecture of PKN2 type of Ser/Thr kinases of Synechocystis. (PDF 22 kb)

Supplementary Figure 21

Domain architecture of ABC1 type of Ser/Thr kinases of Synechocystis. (PDF 18 kb)

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Xu, W., Wang, Y. Sequences, Domain Architectures, and Biological Functions of the Serine/Threonine and Histidine Kinases in Synechocystis sp. PCC 6803. Appl Biochem Biotechnol 188, 1022–1065 (2019). https://doi.org/10.1007/s12010-019-02971-w

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