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Volume 59, Issue 4


Genomic and phylogenetic analysis of Ceramium cimbricum (Ceramiales, Rhodophyta) from the Atlantic and Pacific Oceans supports the naming of a new invasive Pacific entity Ceramium sungminbooi sp. nov.

Jeffery R. Hughey
  • Corresponding author
  • Division of Mathematics, Science, and Engineering, Hartnell College, 411 Central Ave., Salinas, CA 93901, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ga Hun Boo
  • Department of Biology, Chungnam National University, Daejeon 305-764, Korea and University Herbarium, University of California, 1001 Valley Life Sciences Building #2465, Berkeley, CA 94720, USA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2016-07-21 | DOI: https://doi.org/10.1515/bot-2016-0036


The filamentous marine red alga Ceramium cimbricum was described from Denmark, but the name has since been applied to populations worldwide. To determine if C. cimbricum from the Pacific is conspecific with C. cimbricum from the Atlantic, we (1) deciphered an authentic rbcL sequence for the lectotype specimen of C. cimbricum, (2) performed phylogenetic analysis on Pacific and Atlantic C. cimbricum, and (3) assembled and analyzed the complete mitochondrial and plastid genomes of specimens of C. cimbricum from Denmark and California. The lectotype sequence of C. cimbricum was unique and fully resolved with other Atlantic Ceramium species, however, the specimens of C. cimbricum from Denmark, Norway, California, Oregon, and Korea formed a clade with Pacific species. The plastid and mitochondrial genomes of C. cimbricum from Denmark and California were similar in length and gene content, differing by only 67 SNPs and nine gaps for the plastid, and by 100 SNPs and 31 gaps for the mitochondrial genomes. These results support the continued application of the name C. cimbricum to specimens from Denmark, and warrant the naming of a new species, Ceramium sungminbooi sp. nov., native to Asia and introduced to the northeastern Pacific and Europe.

Keywords: Ceramiaceae; genome; invasive; phylogenetics; taxonomy


The marine red algal genus Ceramium Roth is one of the most speciose genera of red algae and includes about 207 species (Boo and Lee 1994, Guiry and Guiry 2016). The genus is widespread, distributed from tropical to boreal coasts around the world (Cho et al. 2003a). Ceramium is characterized by erect and terete filamentous thalli with complete or incomplete cortication, rounded cortical cells, and irregularly shaped periaxial cells (Kylin 1956). Species are traditionally distinguished based on cortication, apex structure, gland cells, presence or absence of adventitious branches, number of periaxial cells, and tetrasporangial location, depth, and cleavage type (Nakamura 1965, Cho et al. 2002).

Ceramium cimbricum H.E. Petersen in Rosenvinge (1924), type locality of Egerslev Røn, Limfjord, Denmark (personal communication J. Rueness in Maggs and Hommersand 1993), is reported worldwide (Guiry and Guiry 2016). It was originally described as red to violet in color with a creeping habit, subdichotomous branching, straight apices, and narrow cortical bands (Rosenvinge 1924). The description was later revised to include vegetative and reproductive details such as four to five periaxial cells, and emergent tetrasporangia (Rueness 1992, Maggs and Hommersand 1993). In the North Pacific, C. cimbricum was first reported from Japan by Tokida (1948), Korea by Kang (1966), Alaska by Wynne (1987), and listed by Maggs and Hommersand (1993) as occurring in the North Pacific, but with a question mark. Ceramium cimbricum was also reported from several bays in Oregon, USA, on the basis of morphological criteria (Cho et al. 2002).

Using a combined phylogenetic analysis of partial LSU and Rubisco spacer sequence data, Skage et al. (2005) showed that C. cimbricum was basally positioned on their tree, sister to Ceramium deslongchampsii Chauvin ex Duby. Their study however did not include a representative of C. cimbricum from the Pacific for comparison. Carlile and Waaland (unpublished) accessioned two sequences of C. cimbricum to GenBank from Sitka, Alaska. Most recently, Kim (2012) recognized C. cimbricum as occurring in Korea, but noted that the Korean plants differed from the Alaskan, Oregon, and Atlantic specimens. Kim (2012) concluded that C. cimbricum consists of several cryptic entities, citing tetrasporangial origin (whorled versus adaxial) and rbcL evidence from Alaskan C. cimbricum as support for the establishment of a new species based on Korean C. cimbricum.

Recent analysis of rbcL sequences of Ceramium sp. from Sausalito, San Francisco Bay, California revealed an exact DNA match to Korean specimens. Preliminary anatomical study indicated that the Ceramium sp. from California shared close structural similarities with C. cimbricum from Korea, Oregon, and Europe (Rueness 1992, Maggs and Hommersand 1993, Cho et al. 2002, Kim 2012). Despite the anatomical and molecular studies of C. cimbricum, its taxonomic status in the north Pacific remains debatable. To determine the correct name to apply to specimens assigned to C. cimbricum from the north Pacific, an rbcL sequence deciphered from the lectotype specimen of C. cimbricum was analyzed against modern specimens from Korea, Oregon, California, Norway, and Denmark, and genome sequencing was performed on the lectotype of C. cimbricum, as well as specimens from Denmark and California, USA.

Materials and methods

DNA extractions, amplification, phylogenetic analysis

DNA extraction, PCR amplification, and sequencing of the Korean specimens were performed as described in Boo et al. (2013). The primers used for amplifying and sequencing these specimens for the rbcL gene were F7, F645, R753, and RrbcS (Freshwater and Rueness 1994, Lin et al. 2001, Gavio and Fredericq 2002). The type material and herbarium specimens from Oregon and California specimens were extracted following the protocol outlined in Lindstrom et al. (2011), adhering to the guidelines proposed by Hughey and Gabrielson (2012). The specimens included in the phylogenetic analysis are listed in Table 1. To determine the appropriate substitution model for the rbcL data, Modeltest 3.7 (Posada and Crandall 1998) was used with the Akaike information criterion (AIC). Based on this analysis, GTR+G+I model was selected for the phylogenetic analyses described here. Maximum likelihood (ML) analysis was performed with RAxML v.7.2.8 (Stamatakis 2006). This analysis used 300 independent tree inferences, applying options of automatically optimized subtree pruning regrafting (SPR) rearrangement and 25 distinct rate categories in the program to identify the best tree. Statistical support for each branch was obtained from 1000 bootstrap replications. Bayesian inference (BI) was executed with MrBayes v.3.2.1 (Ronquist et al. 2012) using metropolis-coupled Markov chain Monte Carlo (MC3). For each matrix, two million generations of two independent runs were performed with four chains, and tree sampling every 100 generations. The burn-in period was identified graphically by tracking the likelihoods at each generation to determine when they reached a plateau. Twenty-five percent of the saved trees were removed, and the remaining 30,002 trees were used to infer Bayesian posterior probabilities (BPP). Both ML and BI trees were rooted with Carpoblepharis flaccida (J.V. Lamouroux) Kützing, Carpoblepharis minima E.S. Barton, Reinboldiella schmitziana (Reinbold) De Toni, and Reinboldiella warburgii (Heydrich) Yoshida et Mikami in Yoshida.

Table 1:

Information on samples used in the present study.

Plastid genome sequencing, assembly, annotation

The genome libraries were constructed using the methods outlined by Hughey et al. (2014). The DNA library was sequenced using Illumina (Illumina Inc., San Diego, CA, USA) 36 bp paired-end analysis with the manufacturer’s protocol via the cBot and HiSeq 2000 by HTGC (http://www.htseq.org/). The data were generated with Illumina’s standard pipeline yielding 17,907,810 (Ceramium cimbricum lectotype), 6,724,270 (California specimen), and 14,045,162 (Denmark specimen) filtered reads, and assembled with the default denovo settings using CLC Cell 4.3.0 (®2015 CLC bio, a QIAGEN Company, Redwood City, CA, USA). The mitochondrial and plastid features were annotated using NCBI ORF-finder and alignments obtained via BLASTX against representative Florideophyceae in GenBank. The tRNAs were identified using the tRNAscan-SE 1.21 web server (Schattner et al. 2005) and rRNAs using the RNAmmer 1.2 server (Lagesen et al. 2007). The GenBank accession numbers for the plastid and mitochondrial genomes of C. cimbricum from Denmark are KR814486 and KU145004, and from California are KR025491 and KU145005, respectively.

Morphological examinations

Specimens for anatomical examination were fixed in a 5% formalin and seawater solution. Snippets and cross sections were taken by hand with a blade and mounted with forceps onto glass slides into the formalin solution. Images and measurements were recorded on a Leica DM500 photomicroscope (Leica Microsystems Inc., Buffalo Grove, IL, USA) with a ICC50 high definition camera.


Morphological analysis

Ceramium sungminbooi J.R. Hughey et G.H. Boo sp. nov. (Figures 1–5)


Thalli rose-pink to red in color, bushy and fan-shaped, globose when submerged, erect, 3–8 cm high and wide, pseudo-dichotomously branched, corticated only at the nodes (Figure 1); apices slightly incurved (Figure 2); the periaxial cells are five in number and the cortical bands consist of two to three layers of small cortical cells; cystocarps 300 μm in diameter, axial or lateral, and are naked or surrounded by two involucral branches (Figure 3); tetrasporangia 30–40 μm in diameter, arising adaxially from periaxial cells, strongly emergent (Figures 4 and 5); antheridia not observed. Female gametophytes mixed-phase containing cystocarps with tetrasporangia occurring on lower parts of the same thallus.

Ceramium sungminbooi sp. nov. (1) Holotype of Ceramium sungminbooi from Jindo, Korea, CNU065811. Scale bar=2 cm. (2–5) Sample from boat docks at Sausalito, San Francisco Bay, CA, USA, UC2050593; (2) apices showing slightly incurved tips. Scale bar=100 μm. (3) Laterally positioned cystocarp. Scale bar=100 μm. (4) Emergent tetrasporangium. Scale bar=50 μm. (5) Adaxially arranged tetrasporangia. Scale bar=100 μm.
Figures 1–5:

Ceramium sungminbooi sp. nov. (1) Holotype of Ceramium sungminbooi from Jindo, Korea, CNU065811. Scale bar=2 cm. (2–5) Sample from boat docks at Sausalito, San Francisco Bay, CA, USA, UC2050593; (2) apices showing slightly incurved tips. Scale bar=100 μm. (3) Laterally positioned cystocarp. Scale bar=100 μm. (4) Emergent tetrasporangium. Scale bar=50 μm. (5) Adaxially arranged tetrasporangia. Scale bar=100 μm.


The species epithet honors Professor Sung Min Boo, a student of Ceramium throughout his career, a dedicated teacher and mentor, and lifelong learner of the algae.


S.M. Boo, G.Y. Cho et E.C. Yang s.n., CNU065811 in CNUK, 28.ii.2002, attached to pebbles on the mudflat at Hoedong, Jindo, Korea, 34°25′20.6″N, 126°20′50.5″E, tetrasporophyte (Figure 1); isotypes: CNU065809, CNU065810.

Representative specimens

Heukeodo, Seosan, Korea, 24.viii.2006 (CNU036904-CNU036905); Hoedong, Jindo, Korea, 28.ii.2002 (CNU034423, CNU065806-CNU065808, CNU065812); Jangpyeongri, Tongyeong, Korea, 5.ii.2015 (CNU066082); Sausalito, San Francisco Bay, California, USA, 27.xi.2014 (UC2050596), 23.xii.2014 (UC2050597), and 28.iii.2015 (UC2050598).

Representative organellar genomes

Mitochondrial – KU145004, KU145005 and plastid – KR814486 and KR025491.

Additional illustrations

Cho et al. (2002), figures 35–56; Kim (2012), figures 33–38.

Molecular analysis

ML and BI phylogenetic analyses using rbcL sequences from Ceramium including the complete sequence from the lectotype specimen of Ceramium cimbricum from Egerslev Røn, Limfjorden, Denmark, Ceramium sungminbooi from Hirsholmene, Denmark, C. sungminbooi from Oslofjord, Norway, and 10 specimens of C. sungminbooi from the north Pacific, generated congruent evolutionary hypotheses (Figure 6, only ML shown here). Ceramium cimbricum formed a moderately supported clade with the Atlantic species (68% bootstrap/0.92 BPP). Ceramium sungminbooi was situated in a strongly supported clade with Ceramium boydenii E.S. Gepp, Ceramium californicum J. Agardh, Ceramium gardneri Kylin, Ceramium sp. from Alaska, and four species of Campylaephora J. Agardh (96% bootstrap/1.0 BPP). Intraspecific sequence variation in C. sungminbooi ranged from 0 to 1 bp for the rbcL sequences. The two specimens of C. sungminbooi from Seosan, Korea differed by 1 bp from the specimens from Denmark, Norway, California, Oregon, and the other collections in Korea. The partial rbcL and rbcL-rbcS intergenic spacer sequence (GenBank AY255473) of C.cimbricum” from Akershus, Snaroya, Norway (Skage et al. 2005) was identical to C. sungminbooi from California and Denmark. Interspecific sequence variation for this clade found that C. sungminbooi differed by 2.4–2.5% from C. californicum, 3.2–3.3% from C. boydenii, 4.8–4.9% from Ceramium sp. from Alaska, and 6.3–6.4% from C. gardneri. The lectotype sequence of C. cimbricum differed by 8.5% from C. sungminbooi.

Maximum likelihood phylogram of the genus Ceramium based on rbcL sequences. Bootstrap supports and Bayesian posterior probabilities (BPP) occur at the nodes. A dash (-) indicates values <50% for bootstrap and <0.90 for BPP.
Figure 6:

Maximum likelihood phylogram of the genus Ceramium based on rbcL sequences. Bootstrap supports and Bayesian posterior probabilities (BPP) occur at the nodes. A dash (-) indicates values <50% for bootstrap and <0.90 for BPP.

The organellar genomes of the lectotype of C. cimbricum were not assembled due to low coverage and a preponderance of reads from epiphytic larvae of Mytilus trossulus (Mytilidae, Bivalvia). However, the complete plastid genomes of C. sungminbooi from Hirsholmene, Denmark and California, USA were deciphered, and were similar in length (171,914 and 171,923 bp, respectively). The plastomes are AT rich (72.4%), and include 224 genes (Table 2). Both contain three ribosomal RNA genes (5S, 16S, 23S), 27 transfer RNAs, 46 ribosomal proteins (19 rps, 27 rpl), 27 ymfs (hypothetical chloroplast proteins), 16 open reading frames, 11 photosystem I, 19 photosystem II, 16 ATP synthase and cytochrome b/f complex, and 11 phycobiliprotein genes. Alignment of the two Ceramium plastomes showed that they differed by only 67 SNPs and nine gaps. The 67 SNPs account for 18 amino acid residue changes in 16 of the 194 coding genes characterized. Ten of the 18 substitutions represented conservative substitutions (amino acid substitutions that are not too dissimilar in their R group chemistry) and eight represented radical substitutions (amino acid substitutions that are dissimilar in their R group chemistry) (Table 3).

Table 2:

Plastid genome content of Ceramium sungminbooi from California and Denmark.

Table 3:

Amino acid residue changes due to mutations in plastid and mitochondrial genes in Ceramium sungminbooi plastomes from California and Denmark.

Two mitochondrial genomes were assembled, but are partial due to an inverted repeat of approximately 700 bp in the mitogenomes of C. sungminbooi specimens from Hirsholmene, Denmark and California, USA. Comparison of the two indicates they are similar in length (24,508 bp for Denmark and 24,494 bp for California). The mitogenomes are AT rich (70.9%), and include 43 genes (Table 4). Both mitogenomes contain two ribosomal RNA genes, 20 transfer RNAs, three ribosomal proteins, ymf39, orf140, and 16 genes involved in electron transport and oxidative phosphorylation. Alignment of the Ceramium mitogenomes identified 100 SNPs and 32 gaps. The 100 SNPs account for 11 amino acid residue changes over five (rpl16, cox3, cob, nad2, orf140) of the 21 coding genes characterized. Three of the 11 substitutions represented conservative substitutions, and eight represented radical substitutions (Table 3). Comparison of the C. cimbricum (Denmark) mitogenome with the C. japonicum mitogenome found 5098 SNPs and 2280 gaps. Alignment of the genes for these two species found 631 amino acid substitutions, of which 245 are conservative substitutions and 386 are radical substitutions. Comparison of cox1 sequences of C. sungminbooi found that those from Denmark and California were identical, but they differed by 2 bp (0.1%) from the Jindo, Korea specimens and by 13–16 bp (0.9–1.1%) from the Tongyeong and Seosan, Korea specimens.

Table 4:

Mitochondrial genome content of Ceramium sungminbooi from California and Denmark.


Ceramium sungminbooi is proposed as a new species to accommodate the Ceramium taxon that is native to Korea and introduced to California, Oregon, Denmark, and Norway. Compared to other Ceramium species from the same phylogenetic clade (Figure 1), C. sungminbooi is recognized by the following characteristics: thalli with pseudo-dichotomous branches, apices that are slightly incurved, 4–5 pericentral cells, three cortical cells per node, emergent tetrasporangia that arise adaxially or whorled, and female gametophytes that are occasionally mixed-phase with tetrasporangia.

Discrimination of Ceramium species using rbcL sequences has been demonstrated by previous studies (Cho et al. 2003a,b, Barros-Barreto et al. 2006, Cho et al. 2008, Yang et al. 2009, Wolf et al. 2011, Won and Cho 2011). In this study rbcL sequences from Korea, Oregon, California, Norway, and Denmark were found to be identical, but highly diverged from the lectotype specimen of C. cimbricum, as well as from other previously published sequences of Ceramium. The two rbcL sequences of Ceramium sp. from Sitka, Alaska, USA do not match C. cimbricum in this study, or any Ceramium sequences in GenBank. Morphological examination and further molecular studies are necessary to describe the Alaskan entity. Phylogenetic analysis of the rbcL sequences of C. sungminbooi from Korea indicates that it is distributed from the west to south coast (Jindo, Seosan, Taean, and Tongyeong). According to Kim (2012), it is also present on the east coast of Korea. The C.cimbricum” reported from Moruran, Japan by Nakamura (1965) likely represents C. sungminbooi, but its identification requires molecular investigation.

Specimens of C. sungminbooi from California, USA were found on the docks amongst yachts and fishing boats in Sausalito growing in association with Sargassum muticum (Yendo) Fensholt and Pachymeniopsis lanceolata (K. Okamura) Y. Yamada ex S. Kawabata. These two species were introduced from Asia into San Francisco Bay during different time periods (Silva 1979, Hughey et al. 2009). Sargassum muticum was first recorded in the bay in 1973 and P. lanceolata in 2009. Ceramium sungminbooi from Tongyeong, Korea was found growing epiphytically on Codium fragile (Suringar) Hariot subsp. tomentosoides (van Goor) Silva. This species of Codium was first collected in San Francisco Bay in 1975 (UC1823751, University Herbarium, University of California, Berkeley). Since C. sungminbooi is widely distributed in Korea and the Californian material shows very little genetic differentiation from the Korean specimens, and C. sungminbooi is associated with invasive species in San Francisco Bay, the Californian specimens are here regarded as representing an invasive population that was likely introduced via hull fouling. The Oregon specimens analyzed in this study were also collected from areas (Coos Bay, Newport, Yaquina Bay) that contain introduced seaweeds from Asia. The oldest invader, S. muticum, was first reported to Coos Bay in 1947, likely as a result of the importation of the Pacific oyster from Japan (Phinney 1977). It is unknown whether C. sungminbooi was introduced to Oregon as a result of oyster mariculture or if it was hull-borne.

In Europe Ceramium sungminbooi was likely introduced via the Japanese oyster, and later spread by vessels. The oyster was first imported to Limfjord, Denmark around 1972 and shortly thereafter to Norway in 1979 (Strand and Vøllstad 1997, Dolmer et al. 2014). As shown in other cases of invasive macroalgae in Europe (Mineur et al. 2012), C. sungminbooi is likely to occur near shellfish farms growing on dead shells and oysters. However, the specimen we obtained from Hirsholmene, Denmark, came from a pristine nature reserve in northernmost Denmark. The other from Norway was collected from Frognerkilen, Oslofjord, from a locality with a high volume of vessel traffic (both specimens were sent to us courtesy of Jan Rueness). While it is not possible to speculate on the provenance of the Denmark material, it seems likely that the Norwegian specimen we analyzed invaded Frognerkilen as a result of hull fouling. Nearby, Gittenberger et al. (2010) concluded that the “rapid population expansion in the Netherlands over recent years may indicate that this species (C. ‘cimbricum’) is exotic, not native to NW Europe”. Gittenberger et al. (2012, 2015) later reported the presence of C.cimbricum” from 18 localities from the Wadden Sea, and listed this species as a probable non-native for NW Europe. Although material from the Dutch coast was not analyzed as part of this study, it seems highly probable that the Wadden Sea specimens are also representative of C. sungminbooi from Asia.

The intraspecific organellar genome variation exhibited between specimens of C. sungminbooi from Denmark and California, USA are similar to those reported for Pyropia perforata (J. Agardh) S.C.Lindstrom (Hughey et al. 2014). They found that the lectotype of P. perforata from San Francisco, California differed from a specimen from La Jolla, California by 185 SNPs and 14 gaps, and another from San Juan Island, Washington by 75 SNPs and one gap for its plastid genome. The plastid genome of C. sungminbooi from Denmark differed by 67 SNPs and nine gaps from the California specimen. For the same specimens cited above, P. perforata from San Francisco differed by 120 SNPs (+8 single nucleotide gaps and three large gaps) and 106 SNPs (+3 single nucleotide gaps and three large gaps) for the mitogenomes. By comparison the two C. sungminbooi mitogenomes differed by 100 SNPs and 32 gaps.

Compared to the published Ceramialean plastid genome, Vertebrata lanosa (L.) T.A. Christensen (Rhodomelaceae, Ceramiales), the length (167,158 bp), gene number (223 genes), organization, and content are similar to the C. sungminbooi specimens analyzed here. The differences are that the C. sungminbooi plastid genomes lack rpl29 (ribosomal protein L29), and V. lanosa lacks ycf26 and ycf37. Comparison of the mitochondrial genomes of C. sungminbooi to other Florideophyceae indicates a high level of gene synteny as documented by Yang et al. (2015). Comparison of C. sungminbooi with C. japonicum Okamura (GenBank KJ398159) shows that the two differ significantly in the tandem tRNA chromosomal region intervening orf140 and rps12. Ceramium sungminbooi contains trnA, trnN, trnV, trnR, trnK, compared to C. japonicum with trnA, trnS, trnR, trnY, trnN, trnV, trnR, trnK.


A new species of Ceramium sungminbooi is proposed for the plants previously recognized from the Pacific as C. cimbricum. Ceramium sungminbooi is confirmed as introduced to Oregon and California in the North Pacific, and to Denmark and Norway in Europe. The rbcL sequence determined from the lectotype specimen of C. cimbricum is unique, and based on phylogenetic analysis is resolved with the Atlantic representatives of the genus. Plastid and mitochondrial genome analysis of C. sungminbooi from Denmark and California revealed a very small number of SNPs, and a high level of gene synteny between both genomes and other Florideophyceae.


This work and the first author’s visit to Korea were supported by Marine Biotechnology Grants from the Korean Government’s Ministry of Oceans and Fisheries. Some of this work was also made possible by a private family trust from Paul W. Gabrielson. We also wish to acknowledge Dr. Pimol Moth for assisting in the collection of Ceramium from Sausalito, California.


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About the article

Jeffery R. Hughey

Jeffery R. Hughey is an instructor of biology at Hartnell College in Salinas, California, USA. He received his PhD in 2001 under Dr. Max Hommersand at the University of North Carolina at Chapel Hill, North Carolina, USA. His research focuses on using DNA from type material of red algae to answer taxonomic questions and to investigate genomic evolution. He also studies, discovers, and identifies introduced marine algae.

Ga Hun Boo

Ga Hun Boo is a postdoctoral researcher at the University Herbarium, University of California, Berkeley, USA. He was awarded a PhD by Chungnam National University for his study of the diversity and evolution of the order Gelidiales (Rhodophyta). His main research interest is the taxonomy, phylogeography and phylogenomics of red algae.

Received: 2016-04-21

Accepted: 2016-06-15

Published Online: 2016-07-21

Published in Print: 2016-08-01

Citation Information: Botanica Marina, Volume 59, Issue 4, Pages 211–222, ISSN (Online) 1437-4323, ISSN (Print) 0006-8055, DOI: https://doi.org/10.1515/bot-2016-0036.

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