1.M.1 The Rz/Rz1 Spanin1 (Rz(1)) Family 

Bacteriophage lambda has four adjacent genes, S, R, Rz and Rz1, dedicated to host cell lysis. S encodes the holin and antiholin and R encodes the endolysin while Rz1 and Rz are an outer membrane lipoprotein (Rz1) and a type II signal anchor protein (Rz).  Together they comprise a spanin. The Rz-Rz1 complex spans the periplasm ane carries out the final step in the process of host lysis. Endolysin-mediated degradation of the cell wall is a prerequisite for conformational changes in the Rz-Rz1 complex leading to the juxtaposition and fusion of the two membranes. Fusion removes the last physical barrier to efficient release of progeny virions (Berry et al. 2008; Rajaure et al. 2015).  The lambda Rz and Rz1 lysis genes are remarkable in that Rz1, encoding the outer membrane lipoprotein, is completely embedded in the +1 register within Rz, which itself encodes the inner membrane protein (Summer et al. 2007; Berry et al. 2012; Berry et al. 2008; Kongari et al. 2018). 1.M.1.1 - 5 are most similar to the lambda phage i_spanin, 1.M.1.6 - 10 are derived from mycobacterial and gordonial phages and are most similar to each other, and 1.M.1.11 - 13 are derived from proteobacteria and are most similar to each other. These proteins are i-spanins. Only 1.M.1.1.1, 1.M.1.1.2 and 1.M.1.1.4 include both spanins (i-spanin and o-spanin) of the system.



This family belongs to the Spanin .

 

References:

Berry, J., E.J. Summer, D.K. Struck, and R. Young. (2008). The final step in the phage infection cycle: the Rz and Rz1 lysis proteins link the inner and outer membranes. Mol. Microbiol. 70: 341-351.

Berry, J., M. Rajaure, T. Pang, and R. Young. (2012). The spanin complex is essential for lambda lysis. J. Bacteriol. 194: 5667-5674.

Khakhum, N., U. Yordpratum, A. Boonmee, U. Tattawasart, J.L. Rodrigues, and R.W. Sermswan. (2016). Identification of the Burkholderia pseudomallei bacteriophage ST79 lysis gene cassette. J Appl Microbiol. [Epub: Ahead of Print]

Kongari, R., M. Rajaure, J. Cahill, E. Rasche, E. Mijalis, J. Berry, and R. Young. (2018). Phage spanins: diversity, topological dynamics and gene convergence. BMC Bioinformatics 19: 326.

Liu, P., X. Dong, X. Cao, Q. Xie, X. Huang, J. Jiang, H. Dai, Z. Tang, Y. Lin, S. Feng, and K. Luo. (2023). Identification of Three Campylobacter Lysins and Enhancement of Their Anti-Escherichia coli Efficacy Using Colicin-Based Translocation and Receptor-Binding Domain Fusion. Microbiol Spectr 11: e0451522. [Epub: Ahead of Print]

Rajaure, M., J. Berry, R. Kongari, J. Cahill, and R. Young. (2015). Membrane fusion during phage lysis. Proc. Natl. Acad. Sci. USA 112: 5497-5502.

Summer, E.J., J. Berry, T.A. Tran, L. Niu, D.K. Struck, and R. Young. (2007). Rz/Rz1 lysis gene equivalents in phages of Gram-negative hosts. J. Mol. Biol. 373: 1098-1112.

Examples:

TC#NameOrganismal TypeExample
1.M.1.1.1

The Spanin1 (Rz; inner membrane, IM)/Spanin2 (Rz1; outer membrane, OM) complex. Spanin1, 153 aas; Spanin2, 60 aas. Together they span the periplasm and mediate fusion of the IM and OM. By doing so, they disrupt the double membrane barrier (Berry et al. 2008; Rajaure et al. 2015; Kongari et al. 2018).

Rz/Rz1 of E. coli phage lambda

 
1.M.1.1.10

Uncharacterized protein, SEA_CAMERICO_42, of 125 aas and 1 N-terminal TMS.

UP of Gordonia phage Camerico

 
1.M.1.1.11

Uncharacterized protein of 122 aas and 1 TMS.

UP of Aminobacter aminovorans

 
1.M.1.1.12

Uncharacterized protein of 122 aas and 1 TMS.

UP of Mesorhizobium tamadayense

 
1.M.1.1.13

Putative phage spanin of 126 aas and 1 N-terminal TMS.

PPS of Mesorhizobium sp.

 
1.M.1.1.2

Rz/Rz1 spanin complex of Burkholderia phage BcepIL02

Proteobacterial virus

Rz/Rz1 of Burkholderia phage BcepIL02
Rz, (171 aas; C5IHR7)
Rz1 (71 aas; C5IHR8)

 

 
1.M.1.1.3

Putative Rz (143 aas; W1IXJ3) inner membrane spanin (i-spanin) of a possible Rz/Rz1 spanin complex of lambdoid prophage Rac. No o-spanin was found, but an adjacent gene (UniProt encodes a 62 aa addiction module toxin, HicA which could be either a o-spanin or a toxin which could be exported via the Rz protein.

Proteobacteria

Rz protein of Xenorhabdus szentirmaii

 

 
1.M.1.1.4

Two component spanin consisting of Rz (IM, 145 aas and 1 TMS) and Rz1 (OM, 61 aas and 1 TMS). 

Spanin of Enterobacteria phage P22 (Bacteriophage P22)

 
1.M.1.1.5

Putative spanin of 164 aas and 1 TMS

Putative spanin of Arsenophonus nasoniae (son-killer infecting Nasonia vitripennis)

 
1.M.1.1.6

Putative phage spanin Rz of 128 aas and 1 N-terminal TMS.

PPS of Mycobacterial phage Ptience, gene 45.

 
1.M.1.1.7

Putative phage spanin, Aminay, of 132 aas and 1 N-terminal TMS.

PPS of Mycobacterial phage spanin, Aminay.

 
1.M.1.1.8

Uncharacterized protein of 107 aas and 1 N-terminal TMS.

UP of Prescottella equi (Rhodococcus equi)

 
1.M.1.1.9

Uncharacterized protein, putative spanin, of 134 aas and 1 N-terminal TMS.

UP of Mycobacterium phage Rope

 
Examples:

TC#NameOrganismal TypeExample
1.M.1.2.1

Rz-like/Rz1-like spanin complex; Rz-like, 148 aas and Rz1-like, 163 aas.

Rz/Rz1 complex of Klebsiella phage KP32

 
1.M.1.2.2

Two component Spanin, eRz/eRz1 of 147 and 74 aas, respectively.

Spanin of Pseudomonas phage Phi15

 
1.M.1.2.3

Spanin pair: i-spanin (gene 18.5; 143 aas; P03803) + o-spanin (gene 18.7; 83 aas; P03788).

Spanin pair of Phage T7

 
1.M.1.2.4

Uncharacterized protein of 162 aas and 1 N-terminal TMS.

UP of Desulfovibrio sp. (coral metagenome)

 
1.M.1.2.5

Uncharacterized protein of 123 aas and 1 N-terminal TMS.

UP of E. coli phage rB

 
Examples:

TC#NameOrganismal TypeExample
1.M.1.3.1

Putative two component spanin (of 109 and 89 aas, each with 1 TMS).

Spanin of Enterobacteria phage phiKMV (Pseudomonas phage phiKMV)

 
1.M.1.3.10

Putative spanin of 248 aas and 0 TMSs

UP of Labrenzia alexandrii

 
1.M.1.3.11

Two component spannin, LysB (R4JGE0)/LysC (R4JDL9) of 146 and 97 aas, respectively.  LysBC can lyse E. coli cells (Khakhum et al. 2016).

LysB/LysC of Burkholderia phage ST79

 
1.M.1.3.12

Uncharacterized protein of 114 aas and 1 TMS.

UP of Acanthocystis turfacea Chlorella virus TN603.4.2

 
1.M.1.3.13

Putative spanin (phage hypothetical protein of Tenacibaculum maritimum) of 115 aas and possibly 1 N-terminal TMS.

Putative spanin of Tenacibaculum maritimum

 
1.M.1.3.14

Spanin complex consisting of inner and outer membrane spanin (i- and o-spanin) components of 162 and 129 aas, respectively.

Spannin of Caulobacter phage phiCbK

 
1.M.1.3.15

Spanin (inner membrane spanin of 168 aas and outer membrane spanin of 126 aas.

Spanin of Caulobacter phage CorColossus

 
1.M.1.3.16

Putative phage spanin of 153 aas and 1 N-terminal TMS.

PPS of Histophilus somni

 
1.M.1.3.17

Phage spanin of 148 aas and 1 N-terminal TMS.

Spanin of Pseudoalteromonas distincta   

 
1.M.1.3.18

Phage spanin Rz of 145 aas and 1 N-terminal TMS, Shewanella frigidmarina strain NCIMB 400,  Gene: Sfri_1672

Spanin Rz of Shewanella frigidmarina strain NCIMB 400

 
1.M.1.3.19

Uncharacterized phage spanin Rz of 114 aas and 1 TMS.

Rz ofAcanthocystis turfacea Chlorella virus TN603.4.2

 

 
1.M.1.3.2

Spanin (i-spanin of 114 aas and o-spanin of 82 aas)

Spanin of Caulobacter phage Percy

 
1.M.1.3.20

Uncharacterized protein HOR29, gp46, of 119 aas with 1 N-terminal TMS.

UP of Pectpbacterium phage PP2  

 
1.M.1.3.21

Uncharacterized protein of 119 aas

UP of Jiella sp. CBK1P-4

 
1.M.1.3.22

Uncharacterized DUF6468 domain-containing protein of 116 aa

UP of Aureimonas sp. AU20

 
1.M.1.3.23

Phage spanin Rz of 111 aa

Rz of Fulvimarina pelagi HTCC2506

 
1.M.1.3.24

Putative phage spanin of 94 aas and 1 TMS from a Xylella phage.

PPS of a Xylella phage

 
1.M.1.3.25

Putative spanin of 124 aas and 1 or 2 TMSs, where the N-terminal TMS is strongly hydrophobic while the secon putative TMS is only moderately hydrophobic.

Putative Rz spanin of Croceibacter phage P2559S

 
1.M.1.3.26

Uncharacterized putative spanin of 107 aas and 2 TMSs, N- and C-terminal.

UP of Chryseobacterium carnipullorum

 
1.M.1.3.27

o-Spanin of 73 aas and 1 N-terminal TMS

o-Spanin of Helicobacter acinonychis strain Sheeba, prophage II, orf25.

 
1.M.1.3.28

Uncharacterized protein of 84 aas and 1 TMS.

UP of Helicobacter suis

 
1.M.1.3.29

Uncharacterized protein of 120 aas and 1 TMS.

UP of Helicobacter suis

 
1.M.1.3.3

Uncharacterized putative spanin protein of 136 aas.

Putative spanin of Burkholderia phage Bp-AMP1

 
1.M.1.3.30

Putative phage spanin of 210 aas with 1 N-terminal TMS.

Pps of Fibrella aestuarina

 
1.M.1.3.31

Putative phage i-spainin of 205 aas and 1 N-terminal TMS.

PPS of Spirosoma terrae

 
1.M.1.3.32

Uncharacterized protein of 192 aas and 1 TMS.

UP of Spirosoma sp. KCTC 72228

 
1.M.1.3.33

Uncharacterized protein of 121 aas and 1 N-terminal TMS.

UP of Cronobacter phage vB_CskP

 
1.M.1.3.34

Putative lipoprotein of 79 aas with one N-terminal TMS. It may be a bacterial lysin (Liu et al. 2023).

LP of Campylobacter hyointestinalis subsp. hyointestinalis

 
1.M.1.3.4

Putative inner membrane i-panin of 90 aas and 1 N-terminal TMS, Rz, and putative outer membrane spanin, o-spanin of 107 aas with 1 N-terminal TMS.

Spanin of Ralstonia phage RSJ2

 
1.M.1.3.5

Putative two component spanin, Rz of 118 aas and Rz1 of 83 aas.

Rz/Rz1 of Burkholderia phage JG068

 
1.M.1.3.6

Spanin Rz/Rz1 pair of 110 and 86 aas, each with 1 N-terminal TMS

Rz/Rz1 of Caulobacter phage Cd1

 
1.M.1.3.7

Rz/Rz1 spanin pair of 142 and 82 aas, respectively.

Rz/Rz1 of Klebsiella pneumoniae

 
1.M.1.3.8

Putative spanin complex with two proteins of 109 and 136 aas, both with an N-terminal TMS.

Spanin of phage APSE-6

 
1.M.1.3.9

Uncharacterized spanin Rz homologue of 224 aas and 1 TMS.

UP of Butyrivibrio sp. AE3004

 
Examples:

TC#NameOrganismal TypeExample
1.M.1.4.10

Uncharacterized spanin of 227 aas and 0 TMSs

UP of Pseudomonas sp. StFLB209

 
1.M.1.4.11

Phage-like spanin of 166 aas and 1 N-terminal TMS.

PS of Albitalea terrae

 
1.M.1.4.12

Uncharacterized protein of 184 aas and 1 N-terminal TMS.

UP of Vibrio vulnificus

 
1.M.1.4.13

Rz/RzI spanin protein of 166 aas and 1 N-terminal TMS.

Rz/RzI of Escherichia phage IME11

 
1.M.1.4.14

Uncharacterized protein, i-spanin 114 of 114 aas and 1 N-terminal TMS.

i-spanin 114 of Stutzerimonas stutzeri

 

 
1.M.1.4.15

i-spanin 114 of 114 aas and 1 N-terminal TMS.

Putative phage spanin of Stutzerimonas stutzeri

 
1.M.1.4.16

Uncharacterized protein of 131 aas and 1 TMS.

UP of Rhizobium leguminosarum

 
1.M.1.4.17

Uncharacterized protein of 108 aas and 1 N-terminal TMS.

UP of Methyloterrigena soli

 
1.M.1.4.18

Uncharacterized protein annotated as a P-loop NTPase superfamily protein of 131 aas and 1 TMS.

UP of Dinoroseobacter phage vB_DshS-R5C

 
1.M.1.4.19

Uncharacterized protein of 113 aas.

UP of Myoviridae

 
1.M.1.4.2

Uncharacterized Rz spanin of 180 aas and 1 TMS.

Rz of Ralstonia solanacearum

 
1.M.1.4.20

Putative phage spanin of 138 aas and 1 N-terminal TMS.

PPS of Pseudomonas phage PAK P5 (Gene: PAK_P500031)

 
1.M.1.4.21

Uncharacterized protein of 123 aas and 1 N-terminal TMS.

UP of Cronobacter phage CR3

 
1.M.1.4.22

Uncharacterized protein of 134 aas and 1 N-terminal TMS.

UP of Cronobacter phage vB_CsaM_GAP31

 
1.M.1.4.23

Uncharacterized protein of 161 aas and 1 N-terminal TMS.

UP of Pseudomonas phage PhiH2

 
1.M.1.4.24

Putative spanin of Pseudomonas phage KPP23, gene 008.

Putative spanin of Pseudomonas phage KPP23

 
1.M.1.4.25

Putative phage spanin of 125 aas and 1 N-terminal TMS.

PPS of Stenotrophomonas maltophilia

 

 
1.M.1.4.26

Putative phage spanin of 134 aas and 1 N-terminal TMS.

PPS of Neisseria meningitidis serogroup B (strain MC58)

 
1.M.1.4.27

Uncharacterized protein of 217 aas and 1 N-terminal TMS.

UP of Yersinia massiliensis

 
1.M.1.4.28

Uncharacterized putative phage spanin Rz of Klebsiella pneumoniae of 211 aas and 1 N-terminal TMS.

Putative spanin of Klebsiella pneumoniae

 
1.M.1.4.29

Putative phage spanin of 133 aas and 1 N-terminal TMS.

PPS of Mesorhizobium sp. L103C120A0

 
1.M.1.4.3

Lysis system i-spanin subunit Rz of 166 aas

UP of Microvirgula aerodenitrificans

 
1.M.1.4.30

Putative phage spanin of 156 aas and 1 N-terminal TMS.

PPS of Oricola thermophila

 
1.M.1.4.31

Putative phage spanin of 120 aas and 1 N-terminal TMS.

PPS of Aeromonas phage CC2 

 
1.M.1.4.32

Uncharacterized protein of 128 aas and 1 N-terminal TMS.

UP of Aeromonas phage Ah1

 
1.M.1.4.33

Uncharacterized putative i-spanin protein of 98 aas.

UP of Vibrio phage VBM1

 
1.M.1.4.34

i-Spanin of 163 aas and 1 N-terminal TMS.

i-Spanin of Vibrio phage SSP002

 
1.M.1.4.4

Annotated as "lysozyme" of 208 aas and 1 N-terminal TMS.  A member of the Pfam Phage_lysis superfamily. However, it appears to be a large spanin and is designated here as an uncharacterized protein (UP) (unpublished observations).

UP of Pseudomonas fluorescens

 
1.M.1.4.5

Probable spanin of 165 aas and 1 N-terminal TMS.

Spanin of Luteibacter sp.

 
1.M.1.4.6

Putative i-spanin of 172 aas with 1 N-terminal TMS. It is from Escherichia phage ECML-117 (UniProt acc # I7ATQ8).

Spanin of Escherichia phage ECML-117

 
1.M.1.4.7

Phage spanin of 165 aas and 1 N-terminal TMS.

PS of Myoviridae sp. (insect metagenome)

 
1.M.1.4.8

Uncharacterized protein of 177 aas and 1 N-terminal TMS.

UP of Sphaerotilus montanus

 
1.M.1.4.9

Putative phage spanin Rz of Sideroxydans lithotrophicus (strain ES-1) of 171 aas and 1 N-terminal TMS (Uni Prot acc # D5CTS4).

PPS12 of Sideroxydans lithotrophicus (strain ES-1)

 
Examples:

TC#NameOrganismal TypeExample
1.M.1.5.1

Outer membrane lipoprotein o-spanin/inner membrane i-spanin complex, pseT.2/pseT.3 (Summer et al. 2007).

Bacterial virus

PseT.2/PseT.3 of enterobacterial phage T4
PseT.2 of 99 aas
PseT.3 of 117 aas

 
1.M.1.5.2

i-spanin/o-spanin of 115/95 aas, respectively, each with an N-terminal TMS.

Spanin of Seratia phage SP1

 
1.M.1.5.3

i-Spanin/o-spanin of 110 aas/116 aas, respectively, both with one N-terminal TMS.

Spanin of Enterobacter phage ENC9

 
1.M.1.5.4

Putative phage R1 spanin protein of 120 aas and 1 N-terminal TMS.

PPS of Pectobacterium phage Arno160

 
1.M.1.5.5

Putative phage i-spanin of 149 aas and 1 N-terminal TMS (Orf046). 

PPS of Escherichia phage vB EcoS AKFV33