Abstract
According to the literature the microfilamentous thalli of lichen-forming ascomycetes
of the genus Psoroglaena are assumed to harbour vivid green “prochlorophyte” cyanobacterial photobionts. As
this would be the first report of terrestrial “prochlorophytes” we investigated the
fine structure and two molecular markers (SSU rDNA and rbcL) of the photobionts of P. stigonemoides (Orange) Henssen and P. epiphylla Lücking. Both Psoroglaena spp. had unicellular green algal photobionts, representatives of the Trebouxiophyceae.
The photobiont of P. stigonemoides is closely related to the non-symbiotic Auxenochlorella protothecoides and to a Chlorella endosymbiont of the freshwater polyp Hydra viridis. The putative photobiont of P. epiphylla may be related to Chlorella luteoviridis, C. saccharophila, and a Pseudochlorella isolate. In contrast to other microfilamentous lichens, which derive their shape
from filamentous green algae or cyanobacterial colonies overgrown and ensheathed by
the fungal partner, Psoroglaena mycobionts position their unicellular photobiont in uni- or multiseriate rows which
strongly resemble the situation in filamentous cyanobacterial colonies.
Key words
Auxenochlorella protothecoides
-
Chlorella luteoviridis
- prochlorophytes -
Psoroglaena epiphylla
-
Psoroglaena stigonemoides
- SSU rDNA -
rbcL.
References
- 1
Ahmadjian V..
A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology,
and identification.
Phycologia.
(1967);
6
127-160
- 2
Aptroot A., Diederich P..
Lichens and lichenicolous fungi from New Guinea.
Bibliotheca Lichenologica.
(1997);
64
220pp
- 3
Aragon G., Sarrion F. J..
Epiphytic verrucariaceae (lichens) in mediterranean Spain.
Nova Hedwigia.
(2003);
77
169-187
- 4
Beck A..
Photobiont inventory of a lichen community growing on heavy-metal-rich rock.
Lichenologist.
(1999);
31
501-510
- 5
Beck A., Koop H. U..
Analysis of the photobiont population in lichens using a single-cell manipulator.
Symbiosis.
(2001);
31
57-67
- 6
Bhattacharya D., Friedl T., Damberger S..
Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion
site lineages in the green algae.
Molecular Biology and Evolution.
(1996);
13
978-989
- 7
Conrad W., Kufferath H..
Addition à la flore algologique de Belgique.
Bulletin de la Société Royale de Botanique de Belgique.
(1912);
49
293-335
- 8
Eriksson O. E..
Psoroglaena cubensis and Flakea papillata gen. et sp. nov., two corticolous lichens with a pantropical distribution.
Systema Ascomycetum.
(1992);
11
11-27
- 9
Friedl T..
Inferring taxonomic positions and testing genus level assignments in coccoid green
lichen algae - a phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae Cl-Nov).
Journal of Phycology.
(1995);
31
632-639
- 10
Friedl T..
Evolution of the polyphyletic genus Pleurastrum (Chlorophyta): inferences from nuclear-encoded ribosomal DNA sequences and motile
cell ultrastructure.
Phycologia.
(1996);
35
456-469
- 11 Friedl T., Büdel B..
Photobionts. Nash, T. H., ed. Lichen Biology. Cambridge; Cambridge University Press (1996): 8-23
- 12
Friedl T., O'Kelly C. J..
Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): evidence from 18S rDNA sequence data and ultrastructure.
European Journal of Phycology.
(2002);
37
373-384
- 13
Friedl T., Zeltner C..
Assessing the relationships of some coccoid green lichen algae and the microthamniales
(Chlorophyta) with 18S ribosomal RNA gene sequence comparisons.
Journal of Phycology.
(1994);
30
500-506
- 14
Gunderson J. H., Elwood H., Ingold A., Kindle K., Sogin M. L..
Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes.
Proceedings of the National Academy of Sciences of the USA.
(1987);
84
5823-5827
- 15
Hafellner J..
Ein Beitrag zur Diversität von lichenisierten und lichenicolen Pilzen im Gebiet der
Gleinalpe (Steiermark, Österreich).
Fritschiana.
(2002);
33
33-51
- 16
Hafellner J., Kalb K..
Bemerkenswerte Flechten und lichenicole Pilze von der Insel Madeira.
Herzogia.
(1992);
9
45-102
- 17
Hafellner J., Maurer W..
Weitere Flechtenfunde im südlichen Burgenland (Österreich).
Mitteilungen des Naturwissenschaftlichen Vereines für Steiermark.
(1994);
124
113-134
- 18
Hanegata N..
Phylogeny of the subfamily Scotiellocystoideae (Chlorophyceae, Chlorophyta) and related
taxa inferred from 18S ribosomal RNA gene sequence data.
Journal of Phycology.
(1998);
34
1049-1054
- 19
Harada H..
Psoroglaena japonica (lichenized Ascomycota, Verrucariaceae), a new species from Chiba-ken, central Japan,
with notes on Psoroglaena.
Lichenology.
(2003);
2
5-10
- 20
Hayden H. S., Waaland J. R..
Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast
and nuclear DNA sequences.
Journal of Phycology.
(2002);
38
1200-1212
- 21 Henssen A.. Eine Revision der Flechtenfamilien Lichinaceae und Ephebaceae. Symbolae
Botanicae Upsalienses XVIII: 1, 123 pp., 23 plates. (1963)
- 22
Henssen A..
Psoroglaena costaricensis, a new lichen species from Costa Rica, and remarks on other taxa of the genus Psoroglaena (Verrucariaceae).
Bibliotheca Lichenologica.
(1995);
57
199-210
- 23 Henssen A., Jahns H. M.. Lichenes. Eine Einführung in die Flechtenkunde. Stuttgart;
Thieme (1973): 467pp
- 24
Hepperle D., Nozaki H., Hohenberger S., Huss V. A. R., Morita E., Krienitz L..
Phylogenetic position of the Phacotaceae within the Chlamydophyceae as revealed by
analysis of 18S rDNA and rbcL sequences.
Journal of Molecular Evolution.
(1998);
47
420-430
- 25
Herrera-Campos M. A., Lücking R., Perez R., Campos A., Colin P. M., Pena A. B..
The foliicolous lichen flora of Mexico. V. Biogeographical affinities, altitudinal
preferences, and an updated checklist of 293 species.
Lichenologist.
(2004 a);
36
309-327
- 26
Herrera-Campos M. D. A., Colin P. M., Pena A. B., Lücking R..
The foliicolous lichen flora of Mexico. III. New species from Volcan San Martin Tuxtla
(Sierra de Los Tuxtlas), Veracruz, with notes on Fellhanera santessonii.
Phyton - Annales Rei Botanicae.
(2004 b);
44
167-183
- 27
Honegger R..
Functional aspects of the lichen symbiosis.
Annual Review of Plant Physiology and Plant Molecular Biology.
(1991);
42
553-578
- 28
Honegger R..
Developmental biology of lichens.
New Phytologist.
(1993);
125
659-677
- 29
Honegger R..
Fine structure of the interaction of Leprocaulon microscopicum with its green algal photobiont, Dictyochloropsis symbiontica.
Bibliotheca Lichenologica.
(2004);
88
201-210
- 30
Honegger R., Brunner U..
Sporopollenin in the cell walls of Coccomyxa and Myrmecia phycobionts of various lichens - an ultrastructural and chemical investigation.
Canadian Journal of Botany.
(1981);
59
2713-2734
- 31
Hoshina R., Kato Y., Kamako S., Imamura N..
Genetic evidence of “American” and “European” type symbiotic algae of Paramecium bursaria Ehrenberg.
Plant Biology.
(2005);
7
526-532
- 32
Huss V. A. R., Ciniglia C., Cennamo P., Cozzolino S., Pinto G., Pollio A..
Phylogenetic relationships and taxonomic position of Chlorella-like isolates from low pH environments (pH < 3.0).
BMC Evolutionary Biology.
(2002);
2
13
- 33
Huss V. A. R., Frank C., Hartmann E. C., Hirmer M., Kloboucek A., Seidel B. M., Wenzeler P.,
Kessler E..
Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta).
Journal of Phycology.
(1999);
35
587-598
- 34
Huss V. A. R., Holweg C., Seidel B., Reich V., Rahat M., Kessler E..
There is an ecological basis for host/symbiont specificity in Chlorella/Hydra symbioses.
Endocytobiosis and Cell Research.
(1994);
10
35-46
- 35
Huss V. A. R., Sogin M. L..
Phylogenetic position of some Chlorella species within the Chlorococcales based upon complete small subunit ribosomal RNA
sequences.
Journal of Molecular Evolution.
(1990);
31
432-442
- 36
Karsten U., Friedl T., Schumann R., Hoyer K., Lembcke S..
Mycosporine-like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta).
Journal of Phycology.
(2005);
41
557-566
- 37
Koch W..
Die Gonidie von Racodium rupestre Pers.
Vorträge aus dem Gesamtgebiet der Botanik, Deutsche Botanische Gesellschaft, Neue
Folge.
(1961);
1
61-64
- 38
Krienitz L., Huss V. A. R., Huemmer C..
Picoplanktonic Choricystis species (Chlorococcales, Chlorophyta) and the misconception of “Nannochloris-like” algae.
Phycologia.
(1996);
35
332-341
- 39
Lewin R. A..
Prochlorophyta as a proposed new division of algae.
Nature.
(1976);
261
697-698
- 40
Lewis L. A., Lewis P. O..
Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta).
Systematic Biology.
(2005);
54
936-947
- 41
Liu C. L., Huang X. H., Wang X. L., Zhang X. C., Li G. Y..
Phylogenetic studies on two strains of Antarctic ice algae based on morphological
and molecular characteristics.
Phycologia.
(2006);
45
190-198
- 42 Maddison W. P., Maddison D. R.. MacClade. Sunderland, Massachusetts, USA; Sinauer
Associates (2002)
- 43
Medlin L., Elwood H. J., Stickel S., Sogin M. L..
The characterization of enzymatically amplified eukaryotic 16S like rRNA coding regions.
Gene.
(1988);
71
491-499
- 44
Müller-Argoviensis J..
Lichenologische Beiträge. XXXV.
Flora.
(1891);
74
371-382
- 64
Nyati S., Scherrer S., Honegger R..
Green algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes).
Lichenologist.
(2007);
- 45
Orange A..
Macentina stigonemoides (Verrucariaceae), a new lichenized species from Great Britain and Ireland.
Lichenologist.
(1989);
21
229-236
- 46
Palenik B., Swift H..
Cyanobacterial evolution and prochlorophyte diversity as seen in DNA-dependent RNA
polymerase gene sequences.
Journal of Phycology.
(1996);
32
638-646
- 47
Pore R. S., Barnett E. A., Barnes W. C., Walker J. D..
Prototheca ecology.
Mycopathologia.
(1983);
81
49-62
- 48
Posada D., Crandall K. A..
MODELTEST: testing the model of DNA substitution.
Bioinformatics.
(1998);
14
817-818
- 49
Rausch H., Larsen N., Schmitt R..
Phylogenetic relationships of the green alga Volvox carteri deduced from small subunit ribosomal RNA comparisons.
Journal of Molecular Evolution.
(1989);
29
255-265
- 50
Rindi F., McIvor L., Guiry M. D..
The Prasiolales (Chlorophyta) of Atlantic Europe: an assessment based on morphological,
molecular, and ecological data, including the characterization of Rosenvingiella radicans (Kutzing) comb. nov.
Journal of Phycology.
(2004);
40
977-997
- 51
Sargent M., Zahn R., Walters B., Gupta R., Kaine B..
Nucleotide sequence of the 18S rDNA from the microalga Nanochlorum eucaryotum.
Nucleic Acids Research.
(1988);
16
4156
- 52
Schmitt I., Lumbsch H. T..
Identification of the photobionts in Trapeliopsis and Pertusaria using SSU ribosomal DNA sequences obtained from PCR amplification with a non-green-algal
primer.
Mycotaxon.
(2001);
78
407-411
- 53
Sherwood A. R., Garbary D. J., Sheath R. G..
Assessing the phylogenetic position of the Prasiolales (Chlorophyta) using rbcL and 18S rRNA gene sequence data.
Phycologia.
(2000);
39
139-146
- 54
Shimada A., Kanai S., Maruyama T..
Partial sequence of ribulose-1,5-bisphosphate carboxylase/oxygenase and the phylogeny
of Prochloron and Prochlorococcus (Prochlorales).
Journal of Molecular Evolution.
(1995);
40
671-677
- 55 Swofford D. L.. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods).
Version 4.0b10. Sunderland, Massachusetts, USA; Sinauer Associates (1998)
- 56 Tavaré S..
Some probabilistic and statistical problems in the analysis of DNA sequences. Miura, R. M., ed. Some Mathematical Questions in Biology - DNA Sequence Analysis. Providence,
Rhode Island; American Mathematical Society (1986): 57-86
- 57
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G..
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment
aided by quality analysis tools.
Nucleic Acids Research.
(1997);
25
4876-4882
- 58 Tschermak-Woess E..
The algal partner. Galun, M., ed. Handbook of Lichenology, Vol. 1. Boca Raton, Florida; CRC Press (1988):
39-92
- 59
Turner S., Burger-Wiersma T., Giovanni S. J., Mur L. R., Pace N. R..
The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts.
Nature.
(1989);
337
380-382
- 60
Vežda A..
Foliicole Flechten aus der Republik Guinea (W-Afrika).
Acta Musei Silesiae, Series.
(1973);
A22
67-90
- 61
Wilcox L. W., Lewis L. A., Fuerst P. A., Floyd G. L..
Group I introns within the nuclear encoded small subunit ribosomal RNA gene of 3 green
algae.
Molecular Biology and Evolution.
(1992);
9
1103-1118
- 62
Yamamoto M., Nozaki H., Miyazawa Y., Koide T., Kawano S..
Relationship between presence of a mother cell wall and speciation in the unicellular
microalga Nannochloris (Chlorophyta).
Journal of Phycology.
(2003);
39
172-184
- 63
Yoshinaga K., Ohta T., Suzuki Y., Sugiura M..
Chlorella chloroplast DNA sequence containing a gene for the large subunit of Ribulose-1,5-bisphosphate
carboxylase/oxygenase and a part of a possible gene for the beta subunit of RNA polymerase.
Plant Molecular Biology.
(1988);
10
245-250
R. Honegger
Institute of Plant Biology
University of Zürich
Zollikerstrasse 107
8008 Zürich
Switzerland
Email: rohonegg@botinst.unizh.ch
Editor: M. Sugita