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Int. J. Biol. Sci. 2007, 3
434
International Journal of Biological Sciences
ISSN 1449-2288 www.biolsci.org 2007 3(7):434-445
©Ivyspring International Publisher. All rights reserved
Research Paper
Phycobilisomes linker family in cyanobacterial genomes: divergence and
evolution
Xiangyu Guan
1, *
, Song Qin
2, *
, Fangqing Zhao
2
, Xiaowen Zhang
2
, Xuexi Tang
1
1. College of Marine Life Science, Faculty of Life Science and Technology, Ocean University of China, 266003, Qingdao, P.R.
China
2. Institute of Oceanology, Chinese Academy of Sciences, 266071, Qingdao, P.R. China
* Contributed equally to this study.
Correspondence to: Dr. Xuexi Tang, tel.: +86 532 82898500; fax: +86 532 82880645; e-mail: mutushicn@yahoo.com.cn
Received: 2007.03.23; Accepted: 2007.11.06; Published: 2007.011.10
Cyanobacteria are the oldest life form making important contributions to global CO
2
fixation on the Earth.
Phycobilisomes (PBSs) are the major light harvesting systems of most cyanobacteria species. Recent availability
of the whole genome database of cyanobacteria provides us a global and further view on the complex structural
PBSs. A PBSs linker family is crucial in structure and function of major light-harvesting PBSs complexes. Linker
polypeptides are considered to have the same ancestor with other phycobiliproteins (PBPs), and might have
been diverged and evolved under particularly selective forces together. In this paper, a total of 192 putative
linkers including 167 putative PBSs-associated linker genes and 25 Ferredoxin-NADP oxidoreductase (FNR)
genes were detected through whole genome analysis of all 25 cyanobacterial genomes (20 finished and 5 in draft
state). We compared the PBSs linker family of cyanobacteria in terms of gene structure, chromosome location,
conservation domain, and polymorphic variants, and discussed the features and functions of the PBSs linker
family. Most of PBSs-associated linkers in PBSs linker family are assembled into gene clusters with PBPs. A
phylogenetic analysis based on protein data demonstrates a possibility of six classes of the linker family in
cyanobacteria. Emergence, divergence, and disappearance of PBSs linkers among cyanobacterial species were
due to speciation, gene duplication, gene transfer, or gene loss, and acclimation to various environmental
selective pressures especially light.
Key words: phycobilisomes, cyanobacteria, linker polypeptides, evolution
1. Introduction
Cyanobacteria are prominent constituents of
marine biosphere that account for a significant
percentage of oceanic primary productivity, and are
among the oldest life forms on the Earth capable of
doing oxygenic photosynthesis about 3.5 billion years
ago, which is similar to the process found in higher
plants [1-2]. As the oldest and major light-harvesting
antennae, PBSs are highly organized complexes of
various PBPs and linker polypeptides (Fig.1.), and are
very diverse in structure and pigment composition in
cyanobacteria, red algae, and the cryptomonads [3-5].
They function in light harvesting and energy
migration toward photosystem II or I reaction centers
in thylakoid membrane, except Gloeobacter violaceus
PCC7421 (Gv) having no thylakoid membrane [6,7].
On one hand, PBSs linkers transfer energy of
PBPs to favor a unidirectional flow of excitation
energy from the peripheral rod of PBSs to the PBSs
core and then from the PBSs core to the photosynthetic
reaction center [8]. On the other, PBSs linkers function
to stabilize PBSs structure and determine positions of
the PBPs within PBSs structure. At the same time,
PBSs linkers also interact directly or indirectly with
the chromophores to cause the PBSs structure changes
that can modulate different PBPs subassemblies and
optimize absorbance characteristics [9-11]. The
structural function of PBSs linkers in PBSs has allowed
cyanobacteria to colonize environments and show a
great diversity in terms of light quantity and quality
[12,13]. Positions of highly conserved PBPs were
determined by the specific linker polypeptides, and it
is possible that linker polypeptides somehow interact
to form a scaffold-like structure within PBSs [14].
Whether or not this is the case, it is possible to
distinguish various PBPs assemblies specifically by
their state of aggregation and by their attachment to
relevant linker polypeptides [15-17]. Tandeau de
Marsac and Cohen-Bazire demonstrated for the first
time that several colorless polypeptides that take
12%–15% of the total stainable proteins of the PBS
components are accounted for linker polypeptides
from eight species of cyanobacteria by SDS-PAGE [18].
The nominated system of linker polypeptides are
according to their locations and molecular masses in
PBSs. Glazer [19] has provided a system of
abbreviations to characterize linker peptides with
respect to their locations and molecular masses in
PBSs: PBSs rod linker (L
R
, 27 to 35 kDa), PBSs rod-core
linker (L
RC
, 25 to 27 kDa), PBSs core linker (L
C,
7.7 to
7.8 kDa), and PBSs core-membrane linker (L
CM
, 70 to
120 kDa) [16,20]. The importance of linker polypeptide
for the assembly of defined complexes and their roles
for tuning spectral characteristics of the complexes has
been well understood [21,22].
Int. J. Biol. Sci. 2007, 3
435
Fig. 1. Structural model of a tricylindrical hemidiscoidal phycobilisome (2, 3). The three sky blue circles represent the
tricylindrical core APC, and two bottom cylinders attach to the thylakoid membrane (grey rectangle) with L
CM
. Six rods are arranged
by PC (blue circle), and PE (red circle), and attached FNR (grass green circle) with L
R
from inner to outer part. L
RC
is the linker
between core and rod. All linkers are represented by yellow discs located in each rod.
FNR, being also considered as linker
polypeptides, transfers electrons from ferredoxin to
NADP
+
to generate NADPH with an average value of
1.3 FNR per PBS, [23,24]. FNR encodes a protein that
is composed of three domains: two C-termainal
domains enough to enzymatic activity of FNR and a
~9kDa N-terminal domain generally homologous to
the small phycocyanin (PC) rod-linker polypeptide
CpcD [23,25]. With the exception of CpcD, it is also
reported that there are similarity between FNR and
other PBSs linkers’ different domains [25,26]. In
contrast to other PBSs-associated linkers (cluster with
PBPs), the γ subunits serving as phycoerythrin (PE)
linker polypeptides are chromophorylated, containing
two types of covalently attached linear tetrapyrrole
chromophores, phycoerythrobilin (PEB), and
phycourobilin (PUB) [27]. Genes of L
CM
and L
RC
polypeptides are on the plastid genome, while genes
ending the γ subunits are present on the nuclear
genome [28,29]. Liu [27] found that no high-degree
sequences homology exists between the γ subunits
and other linker polypeptides, and suggested that
different primary structures in a range of balanced
states still perform similar physiological functions
[30,31]. In red algae, γ subunits that are also the
main chromophorylated components of PBPs and
orderly assembled into other PBPs forming a stable
complex with α and β subunits of PE [32-34].
At present, more and more cyanobacterial
genomes’ database have brought about a great
convenience in search for PBSs linkers using
bioinformatic tools. Here, a comparative genomic
analysis on all the data sequences of PBSs linkers in
the cyanobacteria is presented. Observation on PBSs
linker polypeptides was made in 25 cyanobacteria
additional to some model strain cyanobacteria with
improved method of separation of the PBSs linker
family.
Besides, evolution of linker polypeptides in the
varieties of PBSs was analyzed and specific
connections to PBPs or other linkers were performed
for better understanding the function of PBSs in
different environments.
2. Materials and Methods
Database searching and sequence retrieving
Genomes database were searched at JGI
(http://www.jgi.doe.gov/). Protein sequences of the
PBSs linkers previously described were used as
queries for database. Cyanobacteria species examined
included 25 cyanobacterial genomes (20 complete and
5 ongoing): Anabaena, Nostoc, Gloeobacter,
Trichodesmium, Crocosphaera, Synechocystis,
Synechococcus and Prochlorococcus. All 25 genome
sequences were accessed from IMG
(http://img.jgi.doe.gov/cgi-bin/pub/main.cgi) in
FASTA format. Each protein in this query dataset was
used to search potential novel sequences in all
cyanobacteria species with all available genome
sequences, by using the BLASTP and TBLASTN
programs. Sequences giving better reciprocal BLAST
hits were assumed capable of identifying homologous
counterparts in these species if they could be aligned
up with at least the BLAST-Score > 90 and the E-value
< 1E-10. The search was iterated until convergence,
examined individually, and then aligned with Clustal
X [35]. Sequence identity and similarity were
calculated using BioEdit v5.0 [36]. To elucidate the
complete genomic structure of the PBSs linkers’ genes,
all linkers onto the 20 finished cyanobacterial genomes
were mapped (Fig. 2).
Similar searches were run with the Pfam
domains of the PBSs linker proteins to avoid the
exclusion of highly diverged sequences with just
limited conserved motifs. PFAM [37] and SMART [38]
domain analyses with derived sequences that
employed as queries were then carried out to
eliminate false positives.
Int. J. Biol. Sci. 2007, 3
436
Fig.2. Genomic organization of PBSs linkers in 20 sequenced completely cyanobacterial genomes. Vertical bars show the
locations of PBSs linker genes, with FNR in pink and PBSs linkers except FNR in other colors. PBSs linker genes were mapped onto
the chromosome evenly. Long horizontal line indicates the chromosome. The vertical bar above horizontal line indicates the
transcriptional direction opposite to that below a horizontal line.
Phylogenetic analysis
Multiple sequences were aligned using Clustal X,
and then adjusted manually. To maximize the number
of sites available for analysis, partial sequences and
certain sequences with large deletions were excluded.
To understand the evolutionary relationships of all
PBSs linkers in these cyanobacteria genomes,
neighbor-joining method in MEGA3 [39] and
maximum parsimony method in PHYLIP [40] were
used to construct the phylogenetic tree, in which
confidence levels of each branch were determined by
analyzing 1000 bootstrap replicates.
3. Results and discussion
The PBSs linker family in cyanobacteria
From nominated linkers, PBPs-associated linker
family comprises five groups of linkers with own
locations and molecular masses in the PBSs [19]. Most
of the PBSs linkers are clustered with APC
(allophycocyanin), and PC or PE. Therefore, they are
called APC-associated linker (L
C
), PC- and
PE-associated linker (L
R
) [41,42], while L
RC
and L
CM
are involved in attaching peripheral rods to the APC
cores. BLASTP and TBLASTN programs analyses
show that a total of 192 linkers (159 putative
PBPs-associated linker genes, 8 γ subunits, and 25
FNR genes) were obtained and genes ApcC, CpcC,
CpcD, CpeC, CpeD, CpeE, MpeC, MpeE, PecC, CpcG,
ApcE, and PetH derived from 25 cyanobacterial
genomes in this study (Table 1). The species of 21
cyanobacterial strains, their morphologies, main
features, and habitats, as well as the abbreviations
used at the end of gene names are shown (Table 2).
The number of PBPs-associated linkers in these
cyanobacteria is from 1 to 13, and there are a
maximum number of 13 PBSs linkers in Cw and Tr. γ
subunits as special chromophoric linkers were found
in some marine Synechococcus and three low-light
adapted Prochlorococcus lineages, while other three
sequenced Prochlorococcus have only one type linker
FNR (Table 1). Although no γ subunit has been found
in low-light adapted P13 from database, it may exist
because of the same mode of light-harvesting in other
low-light adapted Prochlorococcus, and γ subunits are
difficult to be found with only
BLASTP as it is in low
sequence homology between γ subunits and other
linkers [34]. The light-harvesting structure including γ
subunit in low-light adapted Prochlorococcus can
acclimatize themselves well to same factors especially
low-light of environment.
Int. J. Biol. Sci. 2007, 3
437
Table 1. Cyanobacterial genes encoding PBSs linkers.
species\Gene
product
APC-associated
PBSs core
linker(LC)
PC,PE-associated
PBSs rod
linker(LR)
PBSs rod-core
linker(LRC)
PBSs core-
membrane
linker(LCM)
γ subunit FNR NO
Nostoc sp. PCC 7120
(N7) (F)
ApcCN7 asr0023 CpcCN7 alr0530
CpcDN7 asr0531
PecCN7 alr0525
CpcG1N7 alr0534
CpcG2N7 alr0535
CpcG3N7 alr0536
CpcG4N7 alr0537
ApcEN7 alr0020 PetHN7 all4121 10
Anabaena variabilis
ATCC29413 (Av) (F)
CpcD3Av
Ava2623
CpcD4Av
Ava2933
CpcD2Av
Ava2932
CpcD1Av
Ava2927
Ava2936
Ava2937
Ava2938
Ava2939
Ava2620 PetHAv Ava0782 10
Nostoc punctiforme
PCC73102 (Np) (D)
CpcD5Np
NpR4840
CpcD1Np
NpF0736,
CpcD2Np
NpF3794
CpcD3Np
NpF5291,
CpcD4Np
NpF5292
CpcD6Np
NpF5293
NpF3811
NpF3795
NpR4843 PetHN7 NpR2751 10
Gloeobacter violaceus
PCC 7421 (Gv) (F)
ApcCGv gsr1248
CpcC1Gv glr0950,
CpcC2Gv gll3219
CpcD1Gv
gsr1266,
CpcD2Gv gsr1267
CpeCGv glr1263,
CpeDGv glr1264
CpeEGv glr1265,
glr2806, glr1262
ApcEGv glr1245
PetHGv gll2295 12
Trichodesmium
erythraeum IMS101
(Tr) (F)
CpcD2Tr
Tery_3647
Tery_4104,
Tery_4105
Pec1Tr Tery_4106,
Pec2Tr Tery_4107
Tery_0999,
Tery_0985
CpcD1Tr
Tery_0986
Tery_2486
Tery_3909
Tery_2209
Tery_2210
PetHTr Tery_3658 13
Crocosphaera
watsonii WH8501
(Cw) (D)
Crocosphaera
watsonii WH8501
CpcD7Cw
Contig357_or4307
CpcD3Cw
Contig361_or5717
CpcD5Cw
Contig362_or6341
CpcD6Cw
Contig166_or0659
PecC1Cw
Contig361_or5719
PecC2Cw
Contig361_or5721
Contig315_or2854
CpcD1Cw
Contig166_or0658
CpcD2Cw
Contig315_or2837
CpcD4Cw
Contig361_or5718
Contig362_or6343 Contig207_or1063 PetHCw
Contig343_or3658
13
Synechocystis sp. PCC
6803
(S6) (F)
ApcCS6 ssr3383 CpcC1S6 sll1580
CpcC2S6 sll1579
CpcDS6 ssl3093
CpcG1S6 slr2051
CpcG2S6 sll1471
ApcES6 slr0335
PetHS6 slr1643 8
Synechococcus sp.
CC9311
(S9) (F)
ApcCS9
sync_2325
CpeD1S9
sync_0511
638114101
sync_0512
CpeCS9
sync_0513
638114105
sync_0516
CpeD2S9
sync_2251
638114104
sync_0515
638114838
sync_1249
CpcG1S9
sync_2488
ApcES9
sync_2321
MpeCS9
sync_0502
PetHS9 sync_1003 12
Synechococcus sp.
WH 8102
(S8) (F)
ApcCS8
SYNW0483
MpeES8 (II)
SYNW1989
MpeDS8 (II)
SYNW2000
CpeCS8 (I)
SYNW1999
CpeES8 (I)
SYNW2001
CpcG1S8
SYNW0314
CpcG2S8
SYNW1997
ApcES8
SYNW0486
MpeCS8
SYNW2010
PetHS8
SYNW0751
10
Int. J. Biol. Sci. 2007, 3
438
Synechococcus sp.
CC9605
(S96) (F)
ApcCS96
Syn_cc96052199
CpcCS96(II)
Syn_cc96051534
CpcD1S96(II)
Syn_cc96050443
CpcD2S96(I)
Syn_cc96050444
Syn_cc96050442
Syn_cc96050446
Syn_cc96052287
CpcGS96
Syn_cc96052579
ApcES96
Syn_cc96052196
Syn_cc96050433 PetHS96
Syn_cc96051917
11
Synechococcus sp.
CC9902
(S99) (F)
CpcD1S99
Syn_cc99020477
CpcD2S99
Syn_cc99021899
Syn_cc99021871,
Syn_cc99021885
Syn_cc99021883,
Syn_cc99020444
Syn_cc99021881
Syn_cc99021003
Syn_cc99020399
Syn_cc99020480
Syn_cc99021895
PetHS99
Syn_cc99020749
12
Synechococcus
elongatus PCC 7942
(S79) (F)
CpcD1S79
Syn_pcc79420325
403100330
Syn_pcc79421049
403100340
Syn_pcc79421050
CpcD2S79
Syn_pcc79421051
403110230
Syn_pcc79422030
403092970
Syn_pcc79420328
PetHS79
Syn_pcc79420978
7
Synechococcus sp.
PCC 6301
(S63) (F)
ApcCS63
syc1188_d
CpcC1S63
syc0498_c
CpcC2S63
syc0499_c
CpcDS63
syc0497_c
CpcGS63
syc2065_d
ApcES63
syc1185_d
PetHS63
syc0566_c
7
Thermosynechococcus
elongatus BP-1 (Te) (F)
ApcCTe tsl0955 CpcCTe tlr1959
CpcDTe tsr1960
CpcG1Te tlr1963
CpcG2Te tlr1964
CpcG4Te tlr1965
ApcETe tll2365 PetHTe tlr1211 8
Synechococcus sp.
WH 7805
(S78) (D)
639019614
WH7805_12498
639020074
WH7805_06646
639020076
WH7805_06656
639020077
WH7805_06661
639019440
WH7805_11638
639020072
WH7805_06636
639019618
WH7805_12518
PetHS78
WH7805_04581
8
Synechococcus sp.
WH 5701
(S57) (D)
638958495
WH5701_15296
638958186
WH5701_05910
638958190
WH5701_05930
638959531
WH5701_08859
638958192
WH5701_05940
638958614
WH5701_15881
638958492
WH5701_15281
638961018
WH5701_00450
PetHS57
WH5701_10210
9
Synechococcus sp.
RS9917
(SRS) (D)
638963552
RS9917_08310
638963041
RS9917_02873
638963045
RS9917_02893
638963039
RS9917_02863
638963429
RS9917_07710
638963555
RS9917_08325
PetHSRS
RS9917_01102
7
Synechococcus sp.
JA-3-3Ab
(SJAb) (F)
ApcCSJAb
CYA_2225
CpcDSJAb
CYA_0218
637872096JAb
CYA_0506
637872115JAb
CYA_0528
CpcCSJAb
CYA_2041
CpcG1SJAb
CYA_0215
637873357JAb
CYA_1814
637873394JAb
CYA_1851
PetHSJAb
CYA_1257
9
Synechococcus sp.
JA-2-3Ba (2-13) (SJBa)
(F)
ApcCSJBa
CYB_1440
CpcD1SJBa
CYB_0941
637874979
CYB_0568
CpcCSJBa
CYB_2737
CpcG1SJBa
CYB_0944
637874843
CYB_0431
PetHSJBa
CYB_2882
7
Prochlorococcus
marinus str. MIT 9313
(P93) (F)
PetHP13
PMT1101
1
Prochlorococcus
marinus sp. NATL2A
(Pn) (F)
MpeCPn
PMN12a1678
PetHPn
PMN12a0675
2
Prochlorococcus
marinus str. MIT 9312
(P12) (F)
PetHP12
Pmt93121086
1
Prochlorococcus
marinus subsp.
CCMP1986 (P86) (F)
PetHP86
PMM1075
1
Prochlorococcus
marinus
str. CCMP 1375 (P75)
(F)
PpeCP75
Pro0345
PetHP75 Pro1123 2
Prochlorococcus
marinus MIT 9211
(P92)
638824638
P9211_07152
PetHP92
P9211_03182
2
Number in all 19 79 40 21 8 25 192
Words in first () of species line are abbreviations; Words in second () of species line are “Genome Completion: [F]inished, [D]raft”.
Int. J. Biol. Sci. 2007, 3
439
Table 2. The species names of the 21 cyanobacterial strains, morphologies, main features, and habitats.
Species Morphology Genome size Linkers (%) LHC Features
Prochlorococcus marinus subsp.
CCMP1986
Unicellular 1760 0.57 Chl a
2
/b
2
Marine; HH
Prochlorococcus marinus str. MIT
9312
Unicellular 1853 0.54 Chl a
2
/b
2
Marine; HH
Prochlorococcus marinus sp.
NATL2A
Unicellular 1937 1.03 Chl a
2
/b
2
Marine; LH
Prochlorococcus marinus str. CCMP
1375
Unicellular 1926 1.04 Chl a
2
/b
2
Marine; LH
Prochlorococcus marinus str. MIT
9313
Unicellular 2327 0.43 Chl a
2
/b
2
Marine; LH
Synechococcus sp. CC9311 Unicellular 2942 4.08 PBSs Marine
Synechococcus sp. WH 8102 Unicellular 2580 3.88 PBSs Marine
Synechococcus sp. CC9902 Unicellular 2358 5.09 PBSs Marine
Synechococcus sp. CC9605 Unicellular 2753 4.00 PBSs Marine
Synechococcus elongatus PCC 7942 Unicellular 2712 2.58 PBSs Freshwater
Synechococcus elongatus PCC 6301 Unicellular 2578 2.72 PBSs Freshwater
Crocosphaera watsonii WH8501 Unicellular 5996 2.17 PBSs Nitrogen-fixing
Synechocystis sp. PCC 6803 Unicellular 3618 2.21 PBSs Freshwater
Trichodesmium erythraeum IMS101 Filamentous 7750 1.68 PBSs Nitrogen-fixing
Nostoc punctiforme PCC73102 Filamentous 7672 1.30 PBSs Heterocystous
Anabaena variabilis ATCC29413 Filamentous 5760 1.74 PBSs Heterocystous
Nostoc sp. PCC 7120 Filamentous 6210 1.61 PBSs Heterocystous
Thermosynechococcus elongatus BP-1 Unicellular 2521 3.17 PBSs Thermophilic
Gloeobacter violaceus PCC 7421 Unicellular 4478 2.68 PBSs No thylakoid
membranes
Synechococcus sp. JA-3-3Ab Unicellular 2813 3.20 PBSs Thermophilic
Synechococcus sp. JA-2-3B'a(2-13) Unicellular 2913 2.75 PBSs Thermophilic
In overall, the basic architecture of PBS is widely
conserved, while PBPs, core structure, and PBSs
linkers diversified greatly across different strains of
cyanobacteria [43]. Moreover, for a single strain, it
depends upon the environmental conditions, such as
nutrient availability, temperature, light quality, and
light intensity [14]. L
C
coexisting with L
CM
is a
single-gene in 19 cyanobacterial genomes except for
five sequenced Prochlorococcus, and L
R
and L
RC
can be
found in different amounts in these 20 cyanobacteria.
All 25 cyanobacteria including Gv without thylakoids
have an FNR.
Multiple copies of L
RC
were identified in
most of referred cyanobacterial species in this study.
However, only one L
RC
was found in Cw, S79, S63,
SJAb, and SJBa (Table 1), and there is no such linker in
Gv and Prochlorococcus. The numbers of PC and
PE-associated rod linkers are also diverse among these
25 cyanobacteria. The composition of PBS in
cyanobacteria and red algae vary in response to
environmental changes in light intensity, light quality
(only cyanobacteria), and nutrient availability [43].
Differences in chromophore composition of
phycobiliproteins result in wavelength-specific
difference in light absorption among species of
cyanobacteria. The assembly of the PBS is mediated by
linker polypeptides, and each trimeric or hexameric
subassembly of PBS contains at least one specific
linker polypeptide, which determines the type,
location, and aggregation state of the PBP within the
rod and also modulates the spectroscopic properties
[34]. Light quality and quantity are among the major
factors affecting the composition of PBSs. In some
cyanobacteria, the relative proportion of PC and PE
can vary within the PBS rods in response to a change
in light climate [5,17], but such complementary
chromatic adaptation is rare among marine
Synechococcus [9,41]. Changes in photon fluxes also
have an effect on the structure of PBS. Marine
cyanobacteria can resist high light stress by decreasing
the content of PBS in cell [44,45], due to a reduction in
surface of thylakoid membranes [46]. Prochlorococcus
and Synechococcus are abundant unicellular
cyanobacteria and major participants in global carbon
cycles. Although Prochlorococcus and Synechococcus are
closely related to each other and often cohabit, they
possess very different photosynthetic light-harvesting
antennas [45,47,48,49]. Synechococcus and the majority
of cyanobacteria use PBSs having 7-12 linkers, while
Prochlorococcus uses a chlorophyll a2 /b2
light-harvesting complex. Differences in absorption
properties and cellular costs between chlorophyll
a2/b2 and PBS antennas differentiate them with own
ecological niche in the ocean [45,50]. Prochlorococcus is
a unicellular cyanobacterium that lacks PBS and
contains chlorophyll b as major accessory pigment,
which enables it to absorb blue light efficiently at
low-light intensity and blue wavelengths
characteristic in deep euphotic zone [50]. P86 and P13
are representatives of high- and low-light adapted
ecotypes. The low light-adapted strain has
significantly more genes than its high light
counterpart such as γ subunits, but neither has
PBSs-associated linkers. As transitional
light-harvesting antennae, γ subunits appeared more
recently than other PBSs-associated linkers and the
linkers (FNR and γ subunits) have some
compensatory function.
Evolution in genus Prochlorococcus would have
evolved towards genome reduction [45]. Specific
genome amplification and diversification have taken
certain place during adaptation of the latter to their
specific environments [45]. The PBSs linker genes
should be one of the reduced genes along with
Prochlorococcus genomes reduction, whereas all
Prochlorococcus strains evolved to use (divinyl-)
chlorophyll a/b-protein complexes as the major
Int. J. Biol. Sci. 2007, 3
440
antenna system [50]. In reverse, there are many PBSs
linkers in the genomes of Synechococcus that is also
considered as genome reduction. Whether such a
reduced genome is a derived state resulting from
progressive gene loss or is an ancestral state are
unclear. The PBSs of open-ocean Synechococcus
cyanobacteria are among the most complex ones
described so far since they possess four types of
constitutive PBPs: APC, PC, and two forms of
phycoerythrin: PEI and PEII. The PE-associated
linkers are divergent to PEI- and PEII-associated
linkers along with PE divergence. In previous studies,
the PBSs and linkers were probably co-evolved from
very early stage [51]. Some PBSs rods have one
combination of three PE-associated linkers (e.g., CpeC,
MpeD, and MpeC), while others would have another
combination (e.g., CpeE, MpeD, and MpeE) [26].
Indeed, PBSs rods are in fact more compact than we
assumed. Cyanobacteria with short PBSs rods may
have a heterogeneous linker composition, which allow
these cyanobacteria to colonize a variety of
light-quantity and light-quality environments. Ting et
al. [2] presented a scenario to explain how
Prochlorococcus antenna evolved in an ancestral
cyanobacterium in iron-limited oceans, resulting in
diversification in Prochlorococcus and marine
Synechococcus lineages from a common PBS-containing
ancestor.
Genomic distribution and sequence analysis of
PBSs linker genes
In many cases, the PBSs-associated linkers and
PBPs as well as enzymes that involved in biosynthesis
or binding of phycobilins are directly adjacent to each
other on chromosome and may form up an operon
that is regulated by a same activator [52,53]. From
these data, 36 gene clusters ranging from 1.5 to 13.2 kb
were found in these cyanobacterial genomes (Fig.3). In
overall, there are 15 APC-associated gene clusters, 12
PC-associated gene clusters, 4 PE with PC or
ambiguous PBPs-associated gene clusters, and 5
ambiguous PBPs-associated gene clusters (Fig.3). Most
PBSs-associated linkers and PBPs often clustered and
transcribed in the same direction, but in the reverse
direction with some enzymes’ genes. The other
linkers’ genes such as FNR are arranged randomly in
the genome. There are also many linkers contiguous to
each other in these genomes such as P99 and Cw
genomic sequences, and they do not assemble into an
operon. Although there are γ subunits in some
Prochlorococcus and Synechococcus, but they do not
form gene clusters with other PBSs linker genes.
APC-associated linker gene clusters exist universally,
and the largest putative operon makes up of PE with
PBPs and enzymes’ genes in S93. Genes encoding PC
or PEC subunits are typically followed by genes
encoding APC-associated linker polypeptides and/or
the genes for chromophore attachment to the alpha
subunit. A L
RC
gene always follows the above operon
and forms a separate transcription unit. The apcC
gene, encoding small linker polypeptide Lc
8.9
, lies
downstream from apcB and apcE genes, and upstream
from apcA gene. apcC gene with apcA/B genes locate
together on a transcriptional unit. As one type of the
terminal acceptors of excitation energy within the
PBSs, apcC is also found in the attachment of PBSs to
the membrane.
The structure of PBSs linker gene clusters varies
among species. Almost of PBSs-associated linkers
form up gene clusters with PBPs, but the number of
CpcG and CpeC, CpeD, and CpeE that are divergent
from a same ancestor is uncertain in gene clusters. In
N7, there are a PC gene cluster constituting of four
CpcG1-4 followed by cpcB/A (C-PC β and chain),
CpcD (PC-associated rod linker), and CpcE/F
(Phycocyanobilin lyase α and β subunit), loaded in a
PE gene cluster adjacently, while in Te a gene cluster
make up of three CpcG1, 2, 4 with CpcB/A and
CpcE/F. Similarly, an obvious diversity of a
PE-cluster existed in Gv, and has three PE-associated
linkers CpeC, CpeD, and CpeE. In S63 and S79, the
duplicated PC genes arrange a tandem repeat unit
with three rod linkers’ genes between cpcB
1
/A
1
and
downstream cpcB
2
/A
2
, cpcE/F set. The occurrence of
several different gene sets in the same type of PBS
component is apparently the result of adaptation of
these organisms to different environmental
conditions, such as light quality and nutrient
availability. Some linkers have been diverged from a
common ancestor along with PBPs divergence and
may be caused by gene duplication or horizontal gene
transfer.
With known morphology of PBSs linker clusters
to construct PBSs, divergence and evolution in
arrangement of PBSs cannot be excluded. For
example, some PBSs might have one combination of
APC-, PC-, and PE-associated linker clusters, while
others would have different combinations (only one or
two PBPs-associated linker clusters). It is possible that
PBSs linker clusters are in fact more compact than we
thought, with short rods having a heterogeneous
linker composition adapted well to changing
environments [46]. In another case, a model strain S81
consists of an APC core and rods that made of one
type of PC and two types of PE (I and II), and gather
into a complicated operon. PEI and PEII can bind both
PUB and PEB in different proportions to light acclimation
[46]. In some cyanobacteria, PBSs rod of only PC is
simpler since it possesses only one complete set of α
and β subunits and two PBSs rod-core linkers (CpcG1
and CpcG2), indicating probably a heterogeneous rod
linker composition [54]. Six [46] hypothesized that
PEII-associated linker would firmly anchor the
proximal PEII disk to the rest of the rod, whereas the
short C-terminus of another PEII-associated linker
makes it more susceptible to release/breakage during
photo acclimation processes.
In S81, S99, and S96, cpeR occurs downstream of
PBPs-associated linkers and genes related with PBSs.
The structure is similar to the operon structure of F.
diplosiphon, and the genes of operon are regulated by
the same activator such as CpeR. CpeR is transcribed
as a part of the cpeCDE operon on an extended
transcript, and required for expression of the cpeB/A
operon. Therefore, it is proposed that at onset of green
light, operons cpeCDESTR and cpeB/A are expressed
in series as a genetic cascade [53]. Maybe the clusters
in S81, S99, and S96 work in the same fashion to that
of the operon in F. diplosiphon. According to known
genes, ambiguous genes function in clusters of S81,
S99, and S96 can be inferred comparatively. This
method can deduce the genes’ function such as cpeS,
and cpcT [55,56], and provide information for
validation in experiment.
Int. J. Biol. Sci. 2007, 3
441
Fig.3. Organization of the gene clusters encoding PBSs and PBSs-associated linkers of 17 cyanobacteria. Arrows represent the
direction of translation, and the relative sizes of operon deduced from analysis of the amino acid sequence. The cyanobacteria names
are given on top of the corresponding region. Yellow arrows indicate the PBSs-associated linker; sky blue, blue, and red arrows
represent APC, PC, and PE, respectively; green arrows mean ambiguous PBPs or PBBs linkers.
Conservation domain analysis of PBSs linker
Ancestral PBPs are probably associated with
same precursor of linker polypeptides. It may be
possible that the linker polypeptides developed from
an earlier (possibly non-globin) ancestor of PBPs
[51,57]. Two additional unique β residues interact
directly with the linker polypeptides, and linker
polypeptides are conserved with β residues locating in
F' and F helices [18]. In N7, we chose a cluster
including PBSs-associated linkers, PBPs, PBPs lyase,
and FNR, which have conversion domains shown in
Fig.4. The amino acids of conversion domains are
generally hydrophobic to form β-sheet. The sequence
alignment of identified extensions from CpcG (1-4)
protein shows that these extensions have 37%-54%
identity and 59%-71% similarity, while the identity
between CpcGs and PBPs, CpcGs and PBPs lyase are
both <10%. The PC-associated linker and
PE-associated linker have also a lower identity of
about 20%. The amino acid sequences have high
sequence identity with each other ranging from 43% to
99% (Fig. 4). The CpcD-like domain of FNR is more
frequently found at the C-terminus of CpcD that
encodes the unique rod-terminating linker protein
L
R
8.9 PC
[26]. Evidenced by this domain’s presence at
the alignment between L
R
8.9 PC
and FNR in N7, the
identity and similarity is only 10% and 14%,
respectively. However, a CpcD-like domain is
consistent with that localization, which is at the
N-terminus of the CpcC proteins and a C-terminus
domain, which is more similar to the PC-associated
linker protein in Gv [26]. The sequence analysis shows
that the identity and similarity between N-region of
CpcA approximately 70 amino acids and CpcD are
16% and 44% in N7, respectively. Especially in
high-light-grown cells, the cpcD gene apparently did
not undergo gene duplication. Therefore, it may
assume that L
R
8.9
functions as rod-terminating linker
polypeptide for ending rods with PC [14]. The CpcG3
protein exhibited a strong resemblance to those of
CpcG4 at 51% in identity and 72% in similarity, for
CpcG1, a 38% identity, and a 59% similarity. CpcG1
with CpcG2 have 53% in identity and 69% in
similarity. Conversion domains massed on the
N-terminal was also observed among these series of
CpcG genes. The sequence alignment in S6 shows that
a large part of N-terminus of CpcG2 is almost identical
to that of CpcG1, while the C-terminal part is highly
diverged from each other [58]. With above values of
alignment, CpcG1 and CpcG2 came from a common
ancestor (I), and CpcG3 and CpcG4 came from
another ancestor (II) in N7. Ancestor I and II
associated with each other, and co-evolved in own
distinct roles since the very beginning.
Int. J. Biol. Sci. 2007, 3
442
Fig.4. Multiple amino acid sequence alignment of the PBSs linkers with PBPs in Nostoc sp. PCC 7120. (A). Sequence
alignments for an opera including pecB, pecC, pecE, pecF, cpcB, cpcA, cpcC, cpcD, cpcE, cpcF, and cpcG1-4 in N7. (B).
Sequence alignments for N-terminal domain of FNR in N7. (C). Sequence alignments for cpcG1-4 in N7. The positions of
similarity and identity are marked in gray and black, respectively.
Phylogenetic analysis
We further investigated the relationship among
these PBSs linkers of these 25 cyanobacteria by
generating an alignment of 192 identified PBSs linker
amino acid sequences followed by generation of an
MP phylogenetic tree (Supplementary Material). The
resultant tree depicts 6 phylogenetic classes of
APC-associated L
C
, PC, PE-associated L
R
, L
RC
, L
CM
, γ
subunit, and FNR. Linkers of APC-associated L
C
, L
RC
,
and L
CM
were assembled in monophyletic group
distinctly according to their sequences and functional
Int. J. Biol. Sci. 2007, 3
443
characteristics. Some PE-associated rod linkers are
assembled into two groups in different branches, and
others disperse throughout the rod linker cluster with
PC-associated linkers. A cluster of PE-associated core
linkers has a close relationship with γ subunits and the
other with L
CM
. Further, APC-associated L
C
may share
a recent common ancestor with CpcD (L
R
). The
phylogenetic tree reveals that the genetic
diversification of all groups involves in a more
complex pattern in gene degeneration and
duplication. The L
RC
(CpcG) of N7, Av, SJAb, SJBa,
and Te form another cluster, and in two branches of
that CpcG1 and CpcG2, CpcG3 and CpcG4 (except
CpcG1 of SJAb and SJBa) are in at least 91% and 98%
bootstrap values, respectively. These four copies
(CpcG1-4) most likely have evolved into a recent
duplication, whereas evolution of CpcG among these
species is more complex with horizontal gene
transfers.
Some ambiguous genes can be divided into these
six classes in high bootstrap values with known PBSs
linkers by phylogenetic analysis. For example, some
innominate PBSs linkers are γ subunits
(Syn_cc96050433, Syn_cc99021895, WH5701_00450),
and they are high homologous with known MpeC
(SYNW2010) in S81. These innominate PBSs linkers
may be homological and have the same functions with
known PBSs linkers such as MpeC. The ambiguous
function genes should be validated in the future.
Although Prochlorococcus has no PBS, the vestiges
of a CpcD-like domain which sequence has diverged
and become shorter and extensively modified are still
recognizable. FNR sequence is possible to be a
potentially interesting evolutionary marker for both
ancient and recent cyanobacteria [14]. The 16s rDNA
sequences from 21 sequenced cyanobacteria were
retrieved from IMG, and FNR was the only linker in
all these cyanobacteria. Therefore, FNR as a PBSs
linker identified in 21 cyanobacteria was also used to
construct the phylogeny to discern the evolutionary
history of the PBSs linker family (Supplementary
Material graph B). Both 16s rDNA and FNR
phylogenetic trees can be divided into two major
unbalanced clades and separated into several
monophyletic clusters with strong bootstrap support.
In phylogenetic tree of FNR, clade I contains 18 FNR
proteins of these 21 cyanobacteria, while clade II
contains only 3 FNR proteins. In clade I,
Prochlorococcus and marine Synechococcus form a
cluster and share a common PBP-containing ancestor,
and may have both diversified at a similar point in
evolution [48]. FNR of S63 and S79 are identical, and
are highly homologous with the branch of FNR in Av,
Np, and N7. In clade II, SJAb sequences share a more
recent common ancestor with SJBa than with other
Synechococcus, and in a group with Gv at the bottom of
both trees except for Te that clusters together in clade
II of 16s rDNA. It is found that these groups of FNR
that correspond to their 16s rDNA phylogeny are
mostly based on the tree topology, but S79, S63, and
Te distribute in different clades from the 16s rDNA
phylogeny. Therefore, most FNR sequences are highly
conservative. The appearance of cyanobacterial FNR
might be due to the speciation, and did not diversify
under selective pressures.
4. Conclusion
The current work on the PBSs linker family
facilitates our understanding on biological functions
and complicated interactions between linker
polypeptides and the PBPs from comparative analysis
on 25 cyanobacteria genomes. 192 putative PBSs linker
genes have been identified from 25 species of
cyanobacteria using BLASTP, TBLASTN and ClustalX.
The gene clusters of 36 PBSs linkers ranging from 1.5
kb to 13.2 kb were found in these cyanobacterial
genomes. The possibilities of six classes of the linker
family were demonstrated. Gene duplication, loss,
shuffling, and/or horizontal transfer appear to have
played important roles during the evolution and
divergence of cyanobacterial PBSs linker
polypeptides. Various environmental factors
especially light acclimation were the primary selective
pressures. Future research will drive the field towards
a deeper understanding on evolutional mechanisms of
photosynthetic light-harvesting complexes in
cyanobacteria and red algae.
Supplementary Material
Unrooted MP tree for PBSs linkers in 25 cyanobacteria and
unrooted NJ trees for 16s rDNA and FNR in 21 cyanobacteria
[http://www.biolsci.org/v03p0434s1.pdf]
Acknowledgement
This work was supported by the Key Project
(KZCX-2-YW-209) of Knowledge Innovation Program
of Chinese Academy of Sciences and Hi-Tech Research
and Development Program (2006AA090303) of China
(863).
Conflict of interest
The authors have declared that no conflict of
interest exists.
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