The taxonomic distinctiveness and cosmopolitan distributions of the red algae
Gelidium crinale
and
G. pusillum
remain unclear. Both species were first described in Devon in southwestern England; namely in Ilfracome for
G. crinale
and Sidmouth for
G. pusillum
. We analyzed mitochondrial
cox
1 and plastid
rbc
L sequences from specimens collected in East Asia, Australia, Europe and North America. In all phylogenetic analyses of
cox
1 and
rbc
L sequences,
G. crinale
was distinct from congeners of the genus. The analyses also revealed a sister relationship with the
G. coulteri
and
G. capense
clade. Nineteen
cox
1 haplotypes were identified for
G. crinale
, and they were likely geographically structured. Despite the distinctiveness in both
cox
1 and
rbc
L datasets, the sister relationship of
G. pusillum
in the genus was not resolved. Our
cox
1 and
rbc
L datasets indicate that
G. crinale
is a cosmopolitan species, found in East Asia, Australia, Europe and North America, while the distribution of
G. pusillum
is restricted to Europe and Atlantic North America. Our results suggest that infraspecific classification of
G. pusillum
may be abandoned.
INTRODUCTION
Gelidium
Lamour. is composed of approximately 127 described species distributed globally along tropical, subtropical, and artic shorelines (Freshwater and Rueness 1994, Shimada et al. 2000, Millar and Freshwater 2005, Kim et al. 2011, in press, Guiry and Guiry 2012). Members of the genus can be the most abundant organisms within intertidal algal assemblages.
Gelidium
is economically important as food, and one of the most promising agar sources in rhodophytes. It has recently been used for industrial paper pulp production in Korea (Seo et al. 2010). However, identification of individual
Gelidium
specimens is notoriously difficult because of the high degree of morphological variation, particularly in the smaller and medium-sized species (Dixon and Irvine 1977
a
).
Gelidium crinale
(Hare
ex
Turner) Gallion and
G. pusillum
(Stackhouse) Le Jolis, which are small and morphologically diverse, are among the most difficult species to identify in red algae, and their distributions are unclear. These species are traditionally recognized as two distinct species (Feldmann and Hamel 1936, Silva et al. 1996), and Womersley and Guiry (1994) found a difference between the types of
G. crinale
and
G. pusillum
. On the contrary,
G. crinale
and
G. pusillum
were merged by Dixon and Irvine (1977
a
, 1977
b
). Seven to nine varieties or formas have been described in each of
G. crinale
and
G. pusillum
(Silva et al. 1996, Guiry and Guiry 2012). The name
G. pusillum
is commonly used for any small tuft-forming
Gelidium
(Silva et al. 1996). Although
G. crinale
and
G. pusillum
are considered as the most widely distributed species in the genus AlgaeBase (Guiry and Guiry 2012), the occurrence of both species in many countries should be reassessed.
In this study we characterized two species, namely
G. crinale
and
G. pusillum
, using two molecular markers. To evaluate the relationship and distribution of
G. crinale
and
G. pusillum
, we analyzed plastid
rbc
L, and mitochondrial
cox
1 including type locality materials. Plastid
rbc
L is commonly used for
Gelidium
phylogeny (Freshwater and Rueness 1994, Freshwater et al. 1995, Shimada et al. 2000, Millar and Freshwater 2005, Nelson et al. 2006, Kim et al. 2011). Recent studies have revealed that mitochondrial
cox
1 is useful for both DNA bar-coding of gelidioid red algae and to examine their distribution patterns (Freshwater et al. 2010, Wiriyadamrikul et al. 2010, Kim et al. 2012). In this study, we included published
rbc
L sequences analyzed from
G. crinale
type material (Freshwater et al. 2010) and samples collected in the
G. pusillum
type locality.
MATERIALS AND METHODS
- Taxon sampling and morphological observation
A total of 18 specimens of
G. crinale
were obtained for this study: 17 collected from 10 locations including China, Hong Kong, Korea, Spain and the UK, and one strain from the culture collection of the University of Texas, UTEX (Appendix A). Ten
G. pusillum
field collections were made at five locations in France, Spain and the UK. Materials for morphological observations were mounted on herbarium sheets, while clean apical parts of the specimens were desiccated in silica gel for DNA extraction. Tissues were sectioned using a freezing microtome (FX-802A; Coper Electronics Co., Ltd., Kanagawa, Japan), and sectioned preparations were stained with 1% aqueous aniline blue. Photographs were taken with an FX-35DX camera (Nikon, Tokyo, Japan) attached to a Vanox AHBT3 microscope (Olympus, Tokyo, Japan). Voucher specimens were deposited at the herbarium of Chungnam National University (CNUK), Daejeon, Korea.
- DNA extraction, sequencing and phylogenetic analyses
Twenty-eight specimens were available for DNA extraction (Appendix A). DNA extraction, PCR amplification, and sequencing are described in Geraldino et al. (2010). Primer pairs for amplification and sequencing of each gene were as follows: for
rbc
L, F7-R753 and F645-RrbcS start (Freshwater and Rueness 1994, Lin et al. 2001, Gavio and Fredericq 2002); and for
cox
1, cox143F-cox11549R (Geraldino et al. 2006) and C622F-C880R (Yang et al. 2008).
Ninety-three
rbc
L sequences including 13 new sequences and 65
cox
1 sequences including 24 new
Gelidium
sequences were collated using the Se-Al version 2.0a11 software (Rambaut 1996) and aligned visually. Outgroup taxa used were representatives from
Gelidiella
Feldmann
et
G. Hamel,
Pterocladia
J. Agardh,
Pterocladiella
Santelices
et
Hommersand, and
Ptilophora
(Suhr) Kützing (Freshwater et al. 1995, Kim et al. 2011).
Maximum likelihood (ML) phylogenetic analysis of
rbc
L was performed using the GTR + Γ + I model implemented in RAxML software (Stamatakis 2006). We used 200 independent tree inferences with the “number of run” option, with default optimized subtree pruning and regrafting (SPR) rearrangement and 25 distinct rate categories to identify the best tree. Statistical support for each branch was obtained from 1,000 bootstrap replications using the same substitution model and RAxML program settings.
Bayesian analyses (BA) were performed for combined and individual datasets with MrBayes v.3.1.1 (Ronquist and Huelsenbeck 2003) using the Metropolis-coupled Markov chain Monte Carlo (MC
3
) with the GTR + Γ + I model. For each matrix, one million generations of two independent runs were performed with four chains and sampling trees every 100 generations. The burn-in period was identified graphically by tracking the likelihoods at each generation to determine whether they reached a plateau. The 15,001 trees for
rbc
L and 22,501 trees for
cox
1 sampled at the stationary state were used to infer the Bayesian posterior probability.
A statistical parsimony network of
cox
1 haplotypes was created using TCS version 1.21 software (Clement et al. 2000). Haplotype and nucleotide diversity measurements were performed using DnaSP software (Rozas and Rozas 1999).
RESULTS
- Molecular analyses
A total of 93 sequences from
Gelidium
and outgroups were aligned using a 1,266-nucleotide (nt) portion of
rbc
L. Variable sites were found at 492 portions (38.9%), and 393 portions (31%) were parsimoniously informative. All GenBank accessions of
G. crinale
from nine countries formed a single monophyletic group with maximum
Maximum likelihood tree of Gelidium using 93 rbcL sequences calculated using the GTR + Γ + I evolution model (-lnL = 10511.506124; substitution rate matrix RAC = 0.951940, RAG = 5.742494, RAT = 1.371355, RCG = 1.258690, RCT = 10.348932, RGT = 1; shape parameter [α] = 1.575834). Maximum likelihood bootstrap values and Bayesian posterior probabilities are shown for each clade. Only bootstrap values ≥50% and ≥0.95 Bayesian posterior probabilities are shown.
Maximum likelihood tree of Gelidium using 65 cox1 sequences calculated using the GTR + Γ + I evolution model (-lnL = 9341.027999; substitution rate matrix RAC = 1.153854, RAG = 10.881554, RAT = 1.077417, RCG = 0.000017, RCT = 20.342285, RGT = 1; shape parameter [α] = 1.101521). Maximum likelihood bootstrap values and Bayesian posterior probabilities are shown for each clade. Only bootstrap values ≥50% and ≥0.95 Bayesian posterior probabilities are shown.
support (
Fig. 1
). The
G. crinale
clade consisted of three subgroup; Asian, Australian, and European / American group. Piarwise divergence of
G. crinale
was up to 2.74%.
G. crinale
was sister to the clade of
G. coulteri
Harvey and
G. capense
(S. G. Gmelin) P. C. Silva (93% for ML and 1.0 for BA). Eleven of
G. pusillum
sequences from France, Norway, Spain, and UK formed a monophyletic group (100% for ML and 1.0 for BA).
A total of 65 sequences from
Gelidium
and three outgroups were aligned using a 1,200 nt region of the
cox
1 gene. Among the 447 (37.3%) variable sites, 400 portions (33.3%) were parsimoniously informative. The topology based on
cox
1 sequences was congruent with the
rbc
L phylogeny (
Fig. 2
). The
cox
1 ML tree showed that all
G. crinale
from eight countries were monophyletic (99% for ML and 1.0 for BA). Twelve
G. pusillum
from France, Norway, Spain, UK, and USA were monophyletic with maximum support.
Because of short sequences of
cox
1 in GenBank, in haplotype analyses, we used 618 nt
cox
1 fragment of
G. crinale
from 28 individuals collected in Australia, China, Hong Kong, Korea, Puerto Rico, Spain, UK, and USA. A total of 19 haplotypes among 33 polymorphic sites (5.3%) were found. Haplotype and nucleotide diversities of
cox
1 within
G. crinale
were 0.912 ± 0.049 (
H
) and 0.014 ± 0.005 (
π
), respectively. The 19 haplotypes were placed in three geographically distinct groups; Asian, Australian, and European / American groups (
Fig. 3
). All haplotypes in Asia were closely related. However, H7 from Hainan, China was linked to H5 (with six missing haplotypes) and to H3 and H4 (with seven missing haplotypes). Haplotypes H9-H11 were found in Australia, and haplotypes H12-H19 were found in Puerto Rico, Spain, UK, and USA.
Eleven
G. pusillum
sequences from France, Norway, Spain, and UK formed a monophyletic group with maximum support. Pairwise divergence of
G. pusillum
was 0.24%. Four haplotypes were found from nine individuals of
G. pusillum
from France, Spain and UK (data not shown). Four specimens from France and UK shared same haplotype. Three short
cox
1 sequences (450 nt long) from NCBI (HQ412445-7) from France, Norway and USA were also dentical.
- Morphology of Gelidium crinale and G. pusillum
Specimens of
G. crinale
confirmed by
cox
1 and
rbc
L are shown in
Fig. 4
. Thalli (
Fig. 4
A & B) from Jeoncheon, Korea and Qingdao, China are purple-red, cartilaginous and composed of terete prostrate axes and erect axes (up to 2 cm high). Specimen from Seoko, Hong Kong (
Fig. 4
C) are terete to flattened distally (up to 550 μm wide). Spanish specimen appears to have cylindrical branches (
Fig. 4
D). Large dome-shaped apical cells are evident at the apices and project over the cortical margin (
Fig. 4
E). Axes and branches consist of cortex and medulla (
Fig. 4
F). Three to five layered cortex consist of small, pigmented, rectangular surface, and oval inner cortical cells. Medulla is composed of large, colourless medullary cells that were intermixed with internal rhizoidal filaments.
G. pusillum
thalli are cartilaginous and prostrate axes are terete, quite regular in diameter, and erect branches (
Fig. 5
A-C). Erect axes arise from the dorsal sides of indeterminate, prostrate axes, are compressed and up to 1.5 cm in height. Branches develop irregularly branching of up to three orders. Dome-shaped apical cells are present at the apices (
Fig. 5
D). Axes and branches consist of cortex and medulla (
Fig. 5
E). The cortex consists of three to four layers of small pigmented cells, whereas the medulla is composed of large colorless cells.
DISCUSSION
- Taxonomy of Gelidium crinale and G. pusillum
Based on both mitochondrial
cox
1 and plastid
rbc
L datasets,
Gelidium crinale
was distinct from
G. pusillum
and other congeners of the genus. All
G. crinale
rbc
L sequences from East Asia, Europe, Australia and North America formed a monophyletic clade with a published sequence (AF308786) from the type material (Freshwater et al. 2010).
G. crinale
specimens from East Asia, Australia and North America corresponded to the description by Feldmann and Hamel (1936), and were identified based on the thalli being caespitose and having cylindrical to compressed prostrate and cylindrical erect axes with filiform branches.
G. crinale
formed a clade with
G. capense
from South Africa and
G. coulteri
from USA. It was difficult to identify a synapomorphic characteristic for these three species.
The intraspecific divergence (0.00-2.74%) of
G. crinale
from Asia, Australasia, Europe and North America is similar to that (up to 2.65%) of the species in previous studies (Freshwater et al. 2010) and that (0.00-2.45%) of
Hypnea flexicaulis
Yamaighi
et
Masuda (Geraldino et al. 2006).
Seven varieties or formas have been described in
G. crinale
; f.
luxurians
Collins (type locality, Pacific Beach, San Diego Co. California) (Collins et al. 1906), var.
lubricum
(Kützing) Hauck, var.
spathulatum
(Kützing) Hauck (Adriatic Sea) (Womersley and Guiry 1994), var.
Nineteen cox1 haplotypes (H1-H19) network of Gelidium crinale from 22 localities in Australia, China, Hong Kong, Korea, Puerto Rico, Spain, UK, and USA. Small grey circles correspond to missing haplotypes and the size of each circle is proportional to the number of individuals analyzed. Numerals in parentheses refer to the number of specimens with identical sequences. AU, Australia; CH, China; ES, Spain; HK, Hong Kong; KR, Korea; PR, Puerto Rico; UK, United Kingdom; USA, United States.
corymbosum
(Kützing) Feldmann
et
G. Hamel (type locality, Mediterranean Sea, Italy) (Feldmann and Hamel 1936), var.
perpusillum
Piccone
et
Grunow (Eritrea, Massawa, Italy) (Piccone 1884), var.
platycladum
W. R. Taylor (type locality, Port Aransas, Texas, USA) (Taylor 1943) and var.
polycladum
(Kützing) Hauck. Of these, var.
corymbosum
, var.
platycladum
, and var.
perpusillum
have been accepted taxonomically in AlgaeBase (Guiry and Guiry 2012).
Our
cox
1 haplotype network revealed geological structure of the
G. crinale
populations, but pairwise divergence (up to 2.74% in
cox
1) is in a range of other species, as mentioned in above. It is therefore difficult to conclude whether our molecular data support infraspecific classification or not. Further sampling is necessary for confirming the infraspecific categories.
G. pusillum
specimens from France, Norway, Spain, and USA formed a monophyletic clade with those collected from the type locality (Sidmouth, Devon, England) in both the
cox
1 and
rbc
L trees.
G. pusillum
is characterized by tufted thalli having compressed, oval, or lanceolate branches (Feldmann and Hamel 1936, Silva et al. 1996). All specimens from UK, France and Spain are similar in having compressed thalli and oval or lanceolate branches. The sister relationship of
G. pusillum
in the genus was not resolved in the
cox
1 and
rbc
L trees.
Of nine varieties or formas described within
G. pusillum
, three are considered as synonyms of the species; var.
conchicolum
Piccone et Grunow (type locality, Massawa, Eritrea, Ethiopia) (Piccone 1884), f.
foliaceum
Okamura (Type locality, Shiso-dima, Seto, Kii Province, Japan) (Okamura 1934), and var.
minusculum
Weber-van Bosse (type locality, Daram Inlet, East coast of Misoöl Island, Indonesia) (Weber-van Bosse 1921) (see AlgaeBase, Guiry and Guiry 2012). However, six have still been flagged in the AlgaeBase; var.
cylindricum
W. R. Taylor (type locality, Bahia San Francisco, Ecuador) (Taylor 1945), var.
mucronatum
P. J. L. Dangeard, var.
pacificum
W. R. Taylor (Isla Santa Maria, Galapagos Islands, Ecuador) (Taylor 1945), f.
pakistancium
Afaq-Husain
et
Shameel (type locality, Gadani, Karachi, Pakistan) (Afaq-Husain and Shameel 1999), var.
pulvinatum
(C. Agardh) Feldmann (type locality, Cadíz, Spain) (Feldmann and Hamel 1936), and var.
simplex
P. J. L. Dangeard (type locality, Marocco) (Dangeard 1949).
The monophyly and low genetic variation (up to 0.24%) of
G. pusillum
reveal that
G. pusillum
is a species with less genetic diversities and indicate the above six varieties or formas may be synonyms of the species or belong to other species. For example, four varieties of
G. pusillum
(e.g., var.
conchicola
, var.
cylindricum
, var.
pacificum
, and var.
pulvinatum
) reported in Korea (Lee 1994, Lee and Kim 1995) have not been found in our recent studies despite many trips in their collection sites (Kim et al. 2011,
Morphology of Gelidium crinale. (A) Specimen collected in Jeoncheon, Korea. (B) Specimen collected in Qingdao, China. (C) Specimen collected in Seoko, Hong Kong. (D) Specimen collected in Cadíz, Spain. (E) A dome-shaped apical cell at the tip of a branchlet. (F) Transverse section of an axis. Scale bars represent: A-D, 5 mm; E, 10 μm; F, 50 μm.
Morphology of Gelidium pusillum. (A) Specimen collected in type locality (Sidmouth, Devon, UK). (B) Specimen collected in Cadíz, Spain. (C) Specimen collected in Caen, France. (D) A dome-shaped apical cell at the tip of a branchlet. (E) Transverse section of an axis. Scale bars represent: A-C, 5 mm; D, 10 μm; E, 50 μm.
Map showing current geographic distribution of Gelidium crinale and G. pusillum based on the present study and previous publications (Freshwater and Rueness 1994, Freshwater et al. 1995, 2010, Shimada et al. 1999, Millar and Freshwater 2005, Kim et al. 2011).
in press). Instead, at least one new species in Korea are likely previously misidentified as variant of
G. pusillum
(Kim et al. in press). Specimen (
Fig. 5
B) from the type locality of
G. pusillum
var.
pulvinatum
, Cadíz, Spain did not reveal variation in molecular data and morphology. Therefore, we suggest that infraspecific classification of
G. pusillum
may be abandoned.
- Distribution of Gelidium crinale and G. pusillum
A distribution map of
G. crinale
and
G. pusillum
is shown in
Fig. 6
. Two interesting biogeographic patterns emerge when considering the overall distribution of both species and their distinct lineages revealed by phylogenetic analyses. The parsimony network of
cox
1 haplotypes revealed a geographic structure (
Fig. 3
); Asian, Australian, and European / American groups. In the Asian group, seven haplotypes were found and closely related. Australian group is quite distinct from Asian, and European / American groups. Specimens from North Carolina, USA and Europe made one group with a single missing haplotype. The genetic connectivity between Europe and north America may be caused by similar oceanographic conditions. Our results indicate that
G. crinale
is a cosmopolitan species, although there are high morphological variations and intraspecific divergences. This result is in agreement with previous studies showing that
G. crinale
is distributed globally (Shimada et al. 1999, Millar and Freshwater 2005, Freshwater et al. 2010)
Contrary to previous studies on its global distribution (e.g., Silva et al. 1996, Guiry and Guiry 2012), our
cox
1 and
rbc
L datasets revealed that
G. pusillum
is likely restricted to Europe and Atlantic North America. Despite basic local alignment search tool (BLAST) search of all sequences registered in GenBank as well as sequences generated in the present study, no accession of
G. pusillum
from Asia, Australia and Pacific North America matched those from Europe. However,
G. pusillum
specimens from Spain and France formed a clade with those from Sidmouth, UK. We suggest that records of
G. pusillum
from Europe and Atlantic North America may be the result of misidentifications, and the specimens filed under
G. pusillum
should be treated with caution. We agree with the views of Millar and Freshwater (2005) that
G. pusillum
, reputed to be cosmopolitan (see Silva et al. 1996, Guiry and Guiry 2012), may be limited to areas around Europe and Atlantic North America.
- Conclusions
Identifications of
G. crinale
and
C. pusillum
based on morphology alone is problematic and usually requires molecular analyses for confirmation. Thus, reports of
G. pusillium
outside from of Europe and Atlantic North America should be treated with caution, and herbarium specimens identified as
G. pusillum
in East Asia, Australia and North America should be re-examined. Although
G. crinale
is common in Europe and other continents, its morphology has been less studied than that of
G. pusillum
(Rueness and Fredriksen 1990, 1998, Fredriksen et al. 1994). Thus, further investigation of the morphology and phenology of
G. crinale
is required.
- Appendix A.
Gelidium crinale and G. pusillum samples used in the present study
Gelidium crinale and G. pusillum samples used in the present study
Continued
Acknowledgements
We thank Jeong Kwang Park for preparing plates of morphology, Juliet Brodie and Keith Hiscock for help in collection trip in Devon, UK and Dr. José Lucas Perez in Cadíz, Spain, respectively. This work was supported by Marine Biotechnology Grants from the Ministry of Land, Transportation Maritime Affairs and Basic Science Grant (2012-0704) of Korean Research Foundation to SMB.
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