Detail description of Lithophyllum okamurae (Lithophylloideae, Corallinales), a widely distributed crustose coralline alga in marine ecosystems
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Abstract: Lithophyllum okamurae is one of the important encrusting coralline algae, which plays important roles as primary producer, carbonate sediment builder, and habitat provider in the marine ecosystems. In this study, L. okamurae was collected from tropical coast of Sanya, and firstly described based on both detailed morph-anatomical characteristics and molecular studies of typic DNA sequences. The structure of the thalli of L. okamurae was pseudoparenchymatous construction with radially organized dimerous organizations in the crustose portion. The pseudoparenchymatous construction were composed of three parts, including 1 to 3 layers of epithelia cells which had flatten to round outermost walls, one layer of square or rectangular cells of the hypothallia and multiple layers of square or elongated rectangular peripheral cells. Palisade cells were observed, and the cells of the contiguous vegetative filaments were connected by secondary pit-connections with cell fusions absent. The carposporangial conceptacles, the spermatangial conceptacles, the bisporangial conceptacles and the tetrasporangial conceptacles were observed, and all these four kinds of conceptacles were uniporate. The spermatangial conceptacles were slightly convex and buried at shallow depths in the thalli tissues, and the carposporangial conceptacles and asexual conceptacles were protruding and conical. Phylogenetic studies based on DNA barcoding markers of 18S rDNA, COI, rbcL and psbA revealed that L. okamurae clustered with the closest relation of L. atlanticum, and formed a distinct branch. Based on the comparative anatomical features and the molecular data, the detailed description of the valid species of L. okamurae was firstly given in this study to provide theoretical basis for algae resources utilization and conservation in marine ecosystems.
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Figure 1. Vegetative structures of Lithophyllum okamurae. a. External morphology of alga individuals growing on rocks, and sloughing cells (sl) in sheets form residual on the crust (white arrow). Scale bar is 3 cm. b. Cross-section showing the pseudoparenchymatous construction of the alga thallus, and conceptacles (white arrow) in it. Scale bar is 5 mm. c. Surface view of the thallus, showing conceptacles (white arrow) distributed on both surface and branches. Scale bar is 5 mm.
Figure 2. Anatomical features of Lithophyllum okamurae. a. Vertical fracture showing the thallus crust with dimerous organization, and unistratose hypothallium (h), perithallium (bracket) and epithallium (e) visible. Scale bar is 50 μm. b. Surface view of polygonal epithallial cells with intact (t) and lost (r) roofs. The outer peripheral parts of epithallial cells with lost roofs were uncalcified. Scale bar is 30 μm. c. Vertical fracture showing primary pit connections (pp) and secondary pit connections (sp) among the filaments in peripheral region of the crusts, and calcium carbonate (cc) deposited in the cell walls, and floridean starch grains (sg) stored in the perithallium cells. Scale bar is 30 μm. d. Palisade cells (white arrow) in perithallium part of the crust. Scale bar is 100 μm. e. Epithallium cells sloughing (sl) in form of face peeling under optical microscope. Scale bar is 10 μm.
Figure 3. Anatomical features of fertile crusts and the conceptacles of Lithophyllum okamurae. a. Cross section through a male plant showing spermatangial conceptacles (white arrow) of different developing stages. Scale bar is 1 mm. b. Two spermatangial conceptacles showing apical oblique divisions forming spermatangia (white arrow), and the spermatangia were releasing from the pore (black arrow). Scale bar is 100 μm. c. A spermatangial conceptacle in elder production stage, where spermatangia were produced on the floor of the conceptacle chamber. Scale bar is 50 μm. d. Cross section through a female plant showing cystocarpic conceptacles (white arrow) of different developing stages. Scale bar is 1 mm. e. A developing cystocarpic conceptacle with several cystocarps (cy) in the chamber. Scale bar is 50 μm. f. A cystocarpic conceptacle which was releasing its cystocarps (cy). Scale bar is 50 μm. g. Cross section through an asexual plant showing tetrasporangial or bisporangial conceptacles (white arrow). Scale bar is 1 mm. h. Surface view of a fertile thallus showing uniporate (white arrow) conceptacles, and a uniporate conceptacle with steepled topped roofs (black arrow). Scale bar is 500 μm. i. A fertile tetrasporophyte thalli with a bisporangial conceptacle (black arrow) and several tetrasporangial conceptacles (white arrow) originated in the crust. Scale bar is 1 mm. j. A bisporangial conceptacle with zonate bisporangia (white arrow) and central columella (c) in the chamber, with the bisporangia was releasing. Scale bar is 50 μm. k. A tetrasporangial conceptacle with zonate bisporangia (white arrow) and central columella (c) in the chamber. Scale bar is 50 μm. l. A bisporangial conceptacle with roof and showing putative zonately arranged bisporangia (bs), and the bisporangia arranged around a prominent central columella. Scale bar is 100 μm. m. A tetrasporangial conceptacle with roof showing putative zonately arranged tetrasporangia, and the tetrasporangia arranged around a prominent central columella (c). Scale bar is 100 μm. n. A tetrasporangial conceptacle which was releasing its tetrasporangia. Scale bar is 50 μm.
Figure 4. Tree constructed with ML for the 18S rDNA alignment. Values at branches represent distance analyses of 1 000 bootstrap replicates (left value) and Bayesian posterior probabilities (right value). Branches lacking values received <50% support. GenBank accession numbers provided. The newly generated sequence was shown in bold.
Figure 5. Tree constructed with ML for the rbcL alignment. Values at branches represent distance analyses of 1 000 bootstrap replicates (left value) and Bayesian posterior probabilities (right value). Branches lacking values received <50% support. GenBank accession numbers provided. The newly generated sequence was shown in bold.
Table 1. Four pairs of primers used to perform the sequences
Primer Sequence Reference 18S-G01 5′-CACCTGGTTGATCCTGCCAG-3′ Harper and Saunders (2001) 18S-G14 5′-CTTGGCAGACGCTTTCGCAG-3′ Harper and Saunders (2001) COI-F 5′-TCAACAAATCATAAAGATATTGG-3′ Saunders (2005) COI-R 5′-ACTTCTGGATGTCCAAAAAAYCA-3′ Saunders (2005) rbcL-090F 5′-CCATATGCYAAAATGGGATATTGG-3′ Yoon et al. (2002) R-rbcS start 5′-TGTGTTGCGGCCGCCCTTGTGTTAGTCTCAC-3′ Yoon et al. (2002) psbA-F 5′-ATGACTGCTACTTTAGAAAGACG-3′ Yoon et al. (2002) psbA-R2 5′-TCATGCATWACTTCCATACCTA-3′ Yoon et al. (2002) 
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Table 2. Comparison of species in genus Lithophyllum that share characteristics with Lithophyllum okamurae (present study)
L.
okamurae
(present study)L.
atlanticum
(1)L.
margaritae
(1)L.
incrustans
(2)L.
incrassatum
(2)L.
neoatalayense
(2)L.
corallinae
(3)L.
kotschyanum
(3)L.
neofarlowii
(3)L.
pygmaeum
(3)L.
yessoense
(3)Substratum rocks, corals and shells free living and on rocks free living rocks and debris rocks rocks or spongites growing on Corallina spp. growing on corals rocks ND ND Epithallium Layer 1–3 1–2 1–4 1 ≥5 1 1 1 3–5 Diameter/μm 4.0–7.0/5.0–9.0 3.0–6.0 5.0–13.0 3.0–4.0 5.0–12.0 4.0–6.0 6.6–8.0 5.0–7.0 5.0–10.0 6.6–8.0 Length/μm 4.0–7.0/3.0–6.0 6.0–11.0 1.5–5.0 3.0–4.0 3.0–5.0 2.0–5.0 3.3–5.0 3.0–5.0 4.0–7.0 3.3–5.0 Hypothallium Layer 1 1 ND 2–3 1 Diameter/μm 7.0–13.0/4.0–7.0 5.5–11.0 3.0–10.0 12.0–15.0 9.0–22.0 6.0–15.0 6.9–9.9 7.0–10.0/5.0–10.0 5.0–6.0 5.0–7.0/5.0–10.0 6.6–9.9 Length/μm 7.0–13.0/13.0–17.0 8.0–17.0 7.0–16.0 9.0–11.0 9.0–22.0 3.0–10.0 19.8–23.1(–30.0) 7.0–10.0/7.0–20.0 10.0–13.2 5.0–7.0/7.0–23.0 5.0–6.6 Peripheral Diameter/μm 8.0–11.0/(5.0–)7.0–8.0 (–10.0) 4.5–10.0 4.0–8.0 3.0–35.0 6.0–12.0 9.0–11.0 6.6–9.9 5.0–13.0 3.3–5.0 8.0–16.0 (–23.0)/6.0–13.0 5.0–7.0 Length/μm 8.0–11.0/(10.0–) 12.0–17.0 (–23.0) 6.5–13.0 4.0–13.0 3.0–9.0 6.0–13.0 9.0–11.0 16.5–26.4 (13.0–)15.0–30.0 (–36.0) 6.6–9.9 35.0–60.0/7.0–22.0 5.0–8.0 Spermatangial Chamber diameter/μm n=15 (123.0–) 138.0–163.0 (–175.0) 156.0–269.0 130.0–221.0 72.6–89.1 125.4–224.5 Chamber height/μm (38.0–) 52.5–62.5 (–80.0) 33.0–52.0 39.0–73.0 42.9–52.8 33.0–46.2 Spermatangia Diameter/μm n=15 (2.6–)3.1–3.7(–4.1) Length/μm 10.5–12.5(–14.1) Carposporangial conceptacles Chamber diameter/μm n=20 (159.6–) 167.5–201.5 (–223.0) 132.0–148.5 Chamber height/μm 82.0–112.0 (–131.0) 66.0–108.9 Carposporangia Diameter n=15 19.3–26.0 23.1–29.7 Length 11.3–17.5 13.2–23.1 Asexual conceptacles Chamber diameter/μm n=20 (170.0–) 240.0–265.0 (–315.0) 315.0–345.0 180.0–220.0 260.0–350.0 208.0–364.0 229.0–252.0 168.3–198.0 270.0–360.0 125.4–165.0 220.0–300.0 138.6–141.9 Chamber height/μm (100.0–)125.0–150.0 90.0–130.0 70.0–95.0 110.0 52.0–130.0 83.0–177.0 99.0–105.6 79.2–105.6 75.0–130.0 66.0–112.2 Tetra/Bisporangia Diameter n=15 9.9–23.1(–28.5) 15.0–33.0 15.0–35.0 20.0–35.0 27.0–38.0 26.0–34.0 16.5–26.4 25.0–33.0 16.5–19.8 26.0–34.0 13.2–36.3 Length (39.0–)39.6–52.8(–73.2) 46.0–68.0 40.0–60.0 45.0–80.0 46.0–65.0 65.0–91.0 49.8–59.4 42.0–50.0 39.6–49.5 50.0–58.0 29.7–66.0
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