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Folia Cryptog. Estonica, Fasc. 48: 135–148 (2011)
INTRODUCTION
For a long time it was considered that the pho-
tobiont composition of lichens was constant.
Questions concerning the origin and constancy
of a photobiont within different lichens ap-
peared about twenty years ago (Friedl, 1987;
Ott, 1987; Ihda et al., 1993; Beck et al., 1998;
Helms, 2003). According to the latest data (Kirk
et al., 2008) the number of lichen-forming fungi
average 17 500 to 20 000 species, while the
number of known photobionts does not exceed
148 species (Voytsekhovich et al., 2011). Sev-
eral levels of mycobiont selectivity have been
established (Beck et al., 2002). Thus, majority
of lichen-forming fungi (approximately 40%) is
-
sociation with only one algal strain (very high
level of selectivity) or a certain species (high level
of selectivity). For instance, Xanthoria parietina
(L.) Th. Fr. forms its thallus with either Trebouxia
arboricola Puymaly, or with the species which
are closely related to this alga (T. arboricola
subclade) (Nyati, 2006); investigated species
of the genus Pertusaria are associated mainly
with Trebouxia potteri Ahmadjian ex Gärtner
(Ahmadjian, 1993), whereas Umbilicaria spe-
cies associate mainly with Trebouxia simplex
Tscherm.-Woess (Beck, 2002; Romeike et al.,
2002).
Some lichen-forming fungi show a middle-
level of selectivity. They form permanent asso-
ciations with the different species of the same
photobiont genus. This level is known for Cla-
donia species (which form the association with
Asterochloris Tscherm.-Woess only – Ahmadjian,
1993; Piercey-Normore & De Priest, 2001; Yahr
et al., 2004), Megalospora (with Dictyochlorop-
sis Geitler em. Tscherm.-Woess – Tschermak-
Woess, 1984), and Collema (with Nostoc Vauch.
Photobiont composition of some taxa of the genera Micarea and
Placynthiella (Lecanoromycetes, lichenized Ascomycota) from
Ukraine
Anna Voytsekhovich, Lyudmila Dymytrova & Olga Nadyeina
M. H. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Kyiv 01601, Ukraine.
E-mail: trebouxia@gmail.com
Abstract: e photobionts of 22 specimens of Placynthiella and Micarea genera were identied. e photobionts of Pla-
cynthiella dasaea (Stirt.) Khodosovtsev, P. icmalea (Ach.) Coppins & P.James, Micarea melanobola (Nyl.) Coppins and M.
misella (Nyl.) Hedl. are reported for the rst time. is is also the rst report about Elliptochloris reniformis (Watanabe)
Ettl & Gärtner, E. subsphaerica (Reisigl) Ettl & Gärtner, Interlum spp. and Neocystis sp. as the photobionts of lichens. e
mycobiont of some taxa of Micarea and Placynthiella can be associated with several algae at the same time. In this case, one
is the primary photobiont (common for all lichen specimens of a certain lichen species) while the others are additional algae
which vary depending on the substratum or the habitat. Elliptochloris and Pseudococcomyxa species are primary photobionts
for the studied taxa of the genus Micarea. e species of Radiococcuus and Pseudochlorella are primary photobionts of the
studied species of Placynthiella. For all investigated lichens the low selectivity level of the mycobiont is assumed.
Kokkuvõte: Perekondade Micarea ja Placynthiella (Lecanoromycetes, lihheniseerunud kottseened) mõnede
taksonite fotobiondi liigiline koosseis Ukrainas
Määrati lihheniseerunud seente Micarea ja Placynthiella 22 eksemplari fotobiondid. Liikide Placynthiella dasaea (Stirt.) Kho-
dosovtsev, P. icmalea (Ach.) Coppins & P.James, Micarea melanobola (Nyl.) Coppins ja M. misella (Nyl.) Hedl. fotobiondid
identitseeriti esmakordselt. Samuti on see esimene teade vetikate Elliptochloris reniformis (Watanabe) Ettl & Gärtner, E.
subsphaerica (Reisigl) Ettl & Gärtner, Interlum spp. and Neocystis sp. esinemisest samblike fotobiondina. Perekondade
Micarea ja Placynthiella mõned taksonid võivad samaaegselt assotsieeruda mitme vetikaga. Sellisel juhul on üks fotobiont
esmane (ühine sama liigi kõigil eksemplaridel), samas kui teised on täiendavad vetikad, mis eksemplariti erinevad, sõltuvalt
substraadist ja kasvukohast. Elliptochloris ja Pseudococcomyxa liigid on esmased fotobiondid perekonna Micarea uuritud
liikides ning Radiococcuus ja Pseudochlorella liigid – perekonna Placynthiella uuritud liikides. Kõikide uuritud samblike puhul
täheldati mükobiondi madalat selektiivsust.
136 Folia Cryptog. Estonica
ex Born. & Flah. – Degelius, 1954). The same
selectivity level is probably common within ceph-
alodial lichens, for instance, Peltigera aphtosa
(L.) Willd. which forms symbiodemes with Nostoc
and Coccomyxa Schmidle (O’Brien et al., 2005).
The lichen-forming fungi that form their
thalli with the photobionts from the same fami-
lies or orders (low selectivity), or even from the
groupings of higher taxonomic levels (very low
relations between the lichen bionts. Thus, the
common examples of low selectivity are the
following: Stereocaulon ramulosum Räuschel,
which associates with cyanobionts Gloeocapsa
Kütz., Nostoc, Scytonema C. Agardh ex Bornet
& Flahault and Stigonema C. Agardh ex Bornet
& Flahault (Lamb, 1951: cit. Tschermak-Woess,
1989), and lichen-forming fungi of Coenogonia-
ceae, Graphidaceae and Roccellaceae families
that form their thalli with the representatives of
Trentepohliaceae family (Rands, 1933, Santes-
son, 1952, Uyenko, 1965: cit. Tschermak-
Woess, 1989; Meier & Chapman, 1983). The very
low selectivity level is common for Verrucaria
Schrad. species that form associations with
Dilabilum prostratum Broady & Ingerfeld (Ettl
& Gärtner, 1995), Diplosphaera chodatii Bial.
(Geitler, 1960: cit. Tschermak-Woess, 1989),
Heterococcus caespitosus Vischer (Tschermak,
1941; Zeitler, 1954; Sanders, 2004), Petroderma
maculiforme (Wollny) Kuckuck (Wynne, 1969;
Moe, 1997; Sanders, 2004), etc. Some of lichen-
ized basidiomycetes can be associated with sev-
eral photobionts at the same time. For instance,
Multiclavula mucida (Pers.) R.H. Petersen was
associated with Mesotaenium Nägeli, Coccomyxa
and Gloeocystis Nägeli (Geitler, 1955).
However, the selectivity levels were ascer-
tained only for 3% of the world lichen diversity
(Voytsekhovich et al., 2011), while the photo-
bionts of remaining 97% of lichen species are
still unknown. Most of the latest publications
on selectivity of the mycobionts deal with the
representatives of certain families of lichens. It
was established that the families Physciaceae
(Bhattacharya et al., 1996; Friedl et al., 2000;
Dahlkild et al, 2001; Helms et al., 2001), Cla-
doniaceae (Piercey-Normore & DePriest, 2001;
Yahr et al., 2004), Teloschistaceae (Beck, 2002;
Honegger et al., 2004; Nyati, 2006), Graphidace-
ae (Nakano, 1988) etc., and genera – Letharia
(Th. Fr.) Zahlbr. (Kroken & Taylor, 2000), Le-
canora Ach. (Blaha et al., 2006) and Umbilicaria
(Romeike et al., 2002) have high and middle
levels of selectivity.
Although, for many lichen species, like e.g.,
Placynthiella Elenkin or Micarea Fr., the data on
photobiont composition are discrepant and still
in need of further investigations. Several pho-
tobionts for the representatives of Placynthiella
have been recorded. For instance, Stigonema
was isolated from Placynthiella arenicola Elenkin
(= P. hyporhoda (Th. Fr.) Coppins & P. James)
(Elenkin, 1912); Gloeocystis sp. (probably, =
Radiococcus Schmidle) (Oxner, 1974) and Coc-
cobotrys lecideae Warén (Ettl & Gärtner, 1995)
– from Placynthiella uliginosa (Schrad.) Coppins
& P. James; Chlorella lichina Chod. (= Chlo-
roidium ellipsoideum (Gerneck) Darienko et al.)
and Nostoc sp. – from Placynthiella sp. (Coppins
& James, 1984); Chlorella sp. was reported for
Placynthiella uliginosa, P. icmalea (Ach.) Coppins
& P. James and P. oligotropha (J.R. Laundon)
Coppins & P. James (Rosentreter et al., 2007).
Besides, Tønsberg (1992) reported several algal
species for the lichen P. dasaea, but did not
indicate their names: the green coccoid photo-
biont up to 12 μm in diameter and additional
algae, which were “2–4-celled, globose or broadly
ellipsoid or more or less cubic, surrounded by
a thick, (3–4 μm wide) gelatinous cap, up to
There are various data concerning the
photobionts of the genus Micarea. According to
Coppins (1983), the photobionts of 45 species
of Micarea
chlorococcoid. Unfortunately, the author gave
only descriptions but no species names for
these algae. The photobiont Pseudochlorella
pyrenoidosa (Zeitler) Lund was isolated from
Micarea assimilata (Nyl.) Coppins (Zeitler, 1954);
Elliptochloris sp. – from M. prasina Fr. (Brunner,
1985). The cyanobionts Nostoc and Stigonema
were also discovered in cephalodia of some
Micarea species (M. assimilata, M. incrassata
Hedl., M. subviolascens (Magnusson) Coppins)
(Coppins, 1983).
The data on photobiont composition often
-
1983; Ahti et al., 1999) require the information
about the type of the photobiont (i.e. trebouxioid,
chlorococcoid or micareoid). Thereby, consider-, consider-consider-
ing the gap in data concerning the photobionts
of lichen species of Micarea and Placynthiella,
137
which are often inconsistent, the investigation
of algal components of these two lichen genera
as well as the analysis of the correlation of their
ecological characters with photobiont composi- characters with photobiont composi-characters with photobiont composi- with photobiont composi-with photobiont composi- photobiont composi-photobiont composi- composi-composi-
tion would be topical and essential, and might
be helpful in clarifying of the problems in biont
interactions.
The aim of the present investigation was
the exploration of algal component of the repre-
sentatives of two lichen genera – Micarea (which
mainly consists of epiphytic bark-growing spe-
cies) and Placynthiella (terricolous and lignicol-
ous species), as well as a comparison and analy-
sis of obtained data in respect to the ecological
peculiarities of these lichen species.
MATERIAL AND METHODS
Lichen samples
Total 22 specimens belonging to 8 species of
Placynthiella and Micarea lichen-forming fungi
were used in the present investigation. Lichen
specimens were collected during 2005–2009
Kherson, Kyiv, Luhansk, and Transcarpathian).
The further information on lichen specimens is
given in Table 1. All lichen specimens are depos-
ited in lichen herbarium of National Academy of
Sciences of Ukraine (KW-L).
Photobionts
Small pieces of lichen thalli were washed in
distilled water. After that the cortical layer of
the thallus was cut out with a sterile razor
blade. Photobionts were isolated directly from
the photobiont layer according to the micropi-
pette method (Ahmadjian, 1993) and grown on
agarized Bold’s medium (3N BBM) in standard
conditions (Friedl & Büdel, 2008): the intensity
of illumination was 10–30 μmol m-2 s-1 PPFD, at
12:12 – light/dark cycle and the temperature
+15±2 °C. After several weeks of cultivation, the
algal strains were investigated in all stages of the
life cycle with the help of the light microscopy
techniques using the microscope Mikmed-2
(LOMO, Russia). The photobionts were exam-
ined both in the lichenized and cultured state
by standard light microscopic techniques. Thus,
the generic level and their percentage in lichen
thalli was conducted in lichenized state using
thallus were studied. Primary photobiont was
-
vestigated specimens of certain lichen species.
Trebouxia
and Asterochloris were compared with cultures
of all known species of these genera, obtained
from culture collections (SAG and CCAP). Cul-
ture strains of the isolated photobionts are
maintained in the algal collection of Department
of Lichenology and Bryology of M.G. Kholodnyi
Institute of Botany (K).
Epiphytes
Epiphytic algae were scrapped from lichen sur-
face on agarized medium in Petri dishes with
the help of sterile preparation needle. After
several weeks of cultivation on agarized Bold’s
medium (3N BBM) in standard conditions (Friedl
& Büdel, 2008), the isolated strains of epiphytic
algae were investigated in all stages of the life
cycle using light microscopy techniques and
compared with photobiont composition of in-
vestigated lichens.
RESULTS
Photobionts
The microscopic study revealed that the speci-
mens of Placynthiella dasaea, Micarea prasina
(No. 19, 20) and M. subnigrata contained only
one photobiont, while the other investigated li-
chen species, Placynthiella icmalea, P. uliginosa,
Micarea melanobola, M. misella, M. peliocarpa
and M. prasina, contained several photobionts
at the same time (Fig. 1a). Later the presence of
help of the cultural methods. The detailed data
concerning photobiont composition of inves-
tigated lichen specimens are given in Table 2.
In seven specimens of Placynthiella uligi-
nosa, as well as in two specimens of P. icmalea,
the photobiont Radiococcus signiensis was
discovered (Fig. 2c). The abundance of this
alga in lichen thalli differed in different speci-
mens. The cells of Radiococcus signiensis in
the specimen of Placynthiella uliginosa (No. 10)
visually presented more than 80% from a total
photobiontal mass, while in the specimen of P.
uliginosa (No. 6) – it was approximately 50%,
and in P. uliginosa (No. 9) – less than 20%. How-
ever, the mycobiont of some of the investigated
thalli of Placynthiella icmalea and P. uliginosa
was associated with other algal species, which
usually were presented in photobiont layer in
138 Folia Cryptog. Estonica
Table 1. Original data of investigated lichen specimens
No. Lichen species Locality in Ukraine, date of specimen collection, and the collector(s)
1Placynthiella dasaea
(Stirt.) Khodosovtsev
Transcarpathian District, Tiachivsky region, Carpathian Biosphere Reserve, Shy-
rokoluzhansky massif, near Posich village, Abies+Fagus woodland, 4821.091'N
43.924'E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova, S. Postoy-.924'E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova, S. Postoy-924'E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova, S. Postoy-'E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova, S. Postoy-E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova, S. Postoy-
alkin & A. Naumovich, det. L. Dymytrova (KW).
2P. dasaea Transcarpathian District, Tiachivsky region, Carpathian Biosphere Reserve, in the
vicinity of Mala Uhol’kaNE, 812 m alt., 9.10.2009, leg. &
det. L. Dymytrova (KW).
3P. icmalea (Ach.)
Coppins & P. James
4638.549'N 3301.185'E, 3 m alt., 01.10.2009, leg. & det. A. Khodosovtsev (KW).
4P. icmalea Transcarpathian District, Tiachivsky region, Carpathian Biosphere Reserve, in the
vicinity of Mala Uhol’kaNE, 812 m alt., 9.10.2009, leg. &
det. L. Dymytrova (KW).
5P. uliginosa (Schrad.)
Coppins & P. James
Luhansk District, Lutugynsky region, in the vicinity of Karl Libkneht’s village,
sandstone outcrops, 03.05.2005, leg. & det. O. Nadyeina (KW45506).
6P. uliginosa Luhansk District, Lutugynsky region, in the vicinity of Verhnya Horikhivka vil-in the vicinity of Verhnya Horikhivka vil-ity of Verhnya Horikhivka vil- of Verhnya Horikhivka vil-Verhnya Horikhivka vil-
(KW45507).
7P. uliginosa Luhansk District, Lutugynsky region, between Myrne village and Uspenka town,
& det. O. Nadyeina
(KW45508).
8P. uliginosa Luhansk District, Lutugynsky region, between Myrne village and Uspenka town,
(KW45509).
9P. uliginosa Luhansk District, Sverdlovsky region, in the vicinity of Provallya village, pasture
land, on soil among mosses, 18.07.2005, leg. & det. O. Nadyeina (KW63536).
10 P. uliginosa Luhansk District, Sverdlovsky region, in the vicinity of Provallya village, steppe
slopes, 22.07.2005, leg. & det. O. Nadyeina (KW45510).
11 P. uliginosa
4638.549'N 3301.185'E, 3 m alt., 01.10.2009, leg. & det. L. Dymytrova (KW).
12 Micarea melanobola
(Nyl.) Coppins
Transcarpathian District, Tiachivsky region, Carpathian Biosphere Reserve, Shy- District, Tiachivsky region, Carpathian Biosphere Reserve, Shy-District, Tiachivsky region, Carpathian Biosphere Reserve, Shy-, Tiachivsky region, Carpathian Biosphere Reserve, Shy-Tiachivsky region, Carpathian Biosphere Reserve, Shy- region, Carpathian Biosphere Reserve, Shy-region, Carpathian Biosphere Reserve, Shy-, Carpathian Biosphere Reserve, Shy-Carpathian Biosphere Reserve, Shy- Biosphere Reserve, Shy-Biosphere Reserve, Shy- Reserve, Shy-Reserve, Shy-, Shy-Shy-
rokoluzhansky massif, near Posich village, m alt.,
05.10.2009, leg. & det. L. Dymytrova (KW).
13 M. misella (Nyl.) Hedl. In the vicinity of '.35'E,
Quercus forest, 02.04.2009, leg. & det. L. Dymytrova (KW).
14 M. peliocarpa (Anzi)
Coppins & R. Sant.
Transcarpathian District, Tiachivsky region, Carpathian Biosphere Reser -
ve, Shyrokoluzhansky massif, near Posich village, Abies-Fagus woodland,
4821.091'N 2343.924'E, 770 m alt., 05.10.2009, leg. O. Nadyeina, L. Dymytrova,
S. Postoyalkin & A. Naumovich, det. L. Dymytrova (KW).
15 M. prasina Fr. Donetsk District, Shakhtars’ky region, in the vicinity of Saurovka village, the dell
& det. O. Nadyeina (KW63549).
16 M. prasina Donetsk District, Shakhtars’ky region, in the vicinity of Petrivs’ke village, steppe
slopes above the dell near tributary of Sevost’yanivka river, 18.04.2006, leg. & det.
O. Nadyeina (KW63539).
17 M. prasina Donetsk District, Shakhtars’ky region, in the vicinity of Petrivs’ke village, along
the dell near tributary of Sevost’yanivka river, solitary Quercus trees, 18.04.2006,
leg. & det. O. Nadyeina (KW63544).
18 M. prasina Donetsk District, Shakhtars’ky region, in the vicinity of Saurivka village, SW di-
rection from Saur-Mohyla, Pinus plantation, 19.04.2006, leg. & det. O. Nadyeina
(KW63550).
19 M. prasina Donetsk District, Shakhtars’ky region, in the vicinity of Saurivka village, SW di-
rection from Saur-Mohyla, Populus+Betula plantation, 19.04.2006, leg. & det. O.
Nadyeina (KW63545).
20 M. prasina Donetsk District, Shakhtars’ky region, the dell “Urochysche Hrabove
20.04.2006, leg. & det. O. Nadyeina (KW63543).
21 M. prasina Luhansk District, Krasnoluchsky region, the dell along Mius river, 19.07.2006,
leg. & det. O. Nadyeina (KW63547).
22 M. subnigrata (Nyl.)
Coppins & H. Kilias
Luhansk District, Sverdlovsky region, sandstone between Dar’yino-Yermakovo
and Astakhovo villages, 22.07.2006, leg. & det. O. Nadyeina (KW 45511).
139
smaller quantity, rather than with the primary
photobiont Radiococcus signiensis. The number
of these algae and their species composition
varied. In most cases, additionally to Radiococ-
cus signiensis the thalli of Placynthiella uliginosa
also contained Elliptochloris subsphaerica (Fig.
3c, d) and Interlum massjukiae (Fig. 2b). Rarely
the members of Asterochloris and Trebouxia
genera were found. One specimen (No. 10) con-
tained Leptosira cf. thrombii. However, not all
of the investigated species of Placynthiella were
associated with Radiococcus. Both specimens of
P. dasaea were associated with the photobiont
Pseudochlorella sp. (Fig. 1c, 2e).
The majority of the investigated specimens of
the genus Micarea contained several photobionts
as well. The exceptions were M. prasina (No.
19, 20) and M. subnigrata, which were associ-
ated with one photobiont only. Nine out of ten
investigated specimens of Micarea contained the
photobionts from the genus Elliptochloris. Thus,
the photobiont Elliptochloris subsphaerica was
found in thalli of Micarea melanobola, M. prasina
(No. 16) and M. subnigrata. The thalli of Micarea
misella, and M. prasina (specimens No. 15, 17,
18, 19, 21) were associated with Elliptochloris bi-
lobata (Fig. 3a, b), while M. peliocarpa contained
Elliptochloris reniformis (Fig. 3e, f). Furthermore,
Fig. 1. Schematical drawings of cuts of Micarea and Placynthiella thalli: (a) photobiont location in
the thallus of Placynthiella uliginosa (scale = 40 μm); (b) Trentepohlia annulata in apothecium of
Micarea misella (scale = 40 μm); (c) lichenized cells of Pseudochlorella sp., surrounded by fungal
hyphae (scale = 10 μm); (d) lichenized Interlum sp. in Micarea thallus (scale = 10 μm).
140 Folia Cryptog. Estonica
Table 2. The photobiont composition of investigated lichen specimens of Micarea and Placynthiella genera compared with literature data.
Lichen
(specimen No.)
Substratum Photobiont Epiphytes
Original data Literature data
Placynthiella
dasaea (No.
1)
decomposed wood of
Abies, covered with
mosses
Pseudochlorella sp.11 Green coccoid photo-
biont and sometimes
additional algae (Tøns-
berg, 1992)
Bracteacoccus giganteus Bisch. & Bold
Chlamydomonas sp.
Elliptochloris bilobata Tscherm.-Woess
Radiococcus signiensis (Broady) Kostikov et al.
Trentepohlia annulata Brand
P. dasaea
(No. 2) decomposed wood of
Abies, covered with
mosses
Pseudochlorella sp. Diplosphaera chodatii Bial.
Interlum terricola (J.B.Petersen) Mikhailyuk et al.
Elliptochloris bilobata
Elliptochloris subsphaerica (Reisigl) Ettl & Gärtner
Pseudococcomyxa sp.
P. icmalea
(No. 3) sand Radiococcus signiensis
Elliptochloris subsphaerica Chlorella sp. (Rosen-
treter et al., 2007)
P. icmalea
(No. 4) dead wood of Pinus tree
(in vicinity of Trapeliop-
sis exulosa)
Radiococcus signiensis
Elliptochloris subsphaerica
Interlum massjukiae Mikhailyuk
et al.
P. uliginosa
(No. 5) mosses (near Amandi-
nea punctata)Radiococcus signiensis
Interlum massjukiae Gloeocystis sp. (Oxner,
1974); Coccobotrys
lecideae Warén (Ettl &
Gärtner, 1995);
Chlorella sp. (Rosen-
treter et al., 2007)
Klebsormidium cf. accidum (Kütz.) Silva et al.
Leptosira cf. thrombii Tscherm.-Woess
Trebouxia sp.
P. uliginosa
(No. 6) soil with crushed rock Radiococcus signiensis
Elliptochloris subsphaerica Asterochloris sp.
P. uliginosa
(No. 7) mosses Radiococcus signiensis
Elliptochloris subsphaerica Interlum massjukiae
Trebouxia sp.
P. uliginosa
(No. 8) mosses (near Cladonia
mbriata)Radiococcus signiensis
Elliptochloris subsphaerica
Interlum massjukiae
Asterochloris sp.
Asterochloris sp.
P. uliginosa
(No. 9) mosses (near Cladonia
foliacea, and Neofusce-
lia pokornyi)
Radiococcus signiensis
Asterochloris cf. excentrica
(Archibald) Skaloud & Peksa
Elliptochloris subsphaerica
Interlum massjukiae
Trebouxia cf. incrustata
Ahmadjian & Gärtner
Diplosphaera chodatii
Parietochloris cf. ovoideus Mikhailyuk et al.
P. uliginosa
(No. 10) thalli of Cladonia co- co-co-
niocraea (near C. folia-. folia-folia-
cea)
Radiococcus signiensis
Asterochloris sp.
Elliptochloris subsphaerica
Interlum massjukiae
Leptosira cf. thrombii
Interlum massjukiae
Leptosira cf. thrombii
P. uliginosa
(No. 11) sand Radiococcus signiensis
Interlum massjukiae
Trebouxia sp.
Klebsormidium cf. accidum
141
Micarea me-
lanobola
(No. 12)
bark of Abies tree Elliptochloris subsphaerica
Pseudococcomyxa sp.
«micareoid» type of
photobiont (Hedlund,
1882, 1895: cit.
Coppins, 1983)
Apatococcus lobatus (Chodat) J.B. Petersen
Trentepohlia cf. umbrina (Kütz.) Bornet
M. misella
(No.13)
decomposed stub Elliptochloris bilobata
Pseudococcomyxa sp
Neocystis sp.
Trentepohlia annulata
M. peliocarpa
(No. 14)
decomposed wood of
Abies
Elliptochloris reniformis
(Watanabe) Ettl & Gärtner
Elliptochloris subsphaerica
«micareoid» type of
photobiont (Hedlund,
1882, 1895: cit.
Coppins, 1983)
Elliptochloris sp.
(Brunner, 1985)
M. prasina
(No. 15)
bark of Fraxinus tree Elliptochloris bilobata
Elliptochloris subsphaerica
Interlum sp.
Trebouxia sp.
M. prasina
(No. 16)
bark of Fraxinus tree Elliptochloris subsphaerica
Interlum sp.
M. prasina
(No. 17)
bark of Quercus tree Elliptochloris bilobata
Elliptochloris subsphaerica
Interlum sp.
M. prasina
(No. 18)
bark of Betula tree Elliptochloris bilobata
Interlum sp.
M. prasina
(No. 19)
bark of Betula tree Elliptochloris bilobata
M. prasina
(No. 20)
bark of Fraxinus tree Pseudococcomyxa sp.
M. prasina
(No. 21)
bark of Betula tree
(near Lecanora hagenii,
Melanelia sp., and Scoli-
ciosporum chlorococcum)
Elliptochloris bilobata
Interlum sp.
Apatococcus lobatus
M. subnigra-. subnigra-subnigra-
ta (No. 22)
on Candelariella vitel- vitel-vitel-
lina (near Rhizocarpon
distinctum, Bellemerea
cupreoatra, Acarospora
fuscata, Sarcogyne re-
gularis)
Elliptochloris subsphaerica «micareoid» type of
photobiont (Hedlund,
1882, 1895: cit.
Coppins, 1983)
The main photobiont of lichen is in bold.
142 Folia Cryptog. Estonica
in the thalli of Micarea melanobola, M. misella
and M. prasina (No. 15, 16, 17, 18, 21) several
additional photobionts were discovered (see
Table 2). For instance, Neocystis sp. was found
and recognized as an additional photobiont of
M. misella; Pseudococcomyxa sp. (Fig. 2f) – as
additional photobiont of Micarea melanobola, M.
misella and M. prasina (No. 20). The majority of
the specimens also contained Interlum sp. (Fig.
2a), which differs from Interlum massjukiae
conditions.
Fig. 2. Photobionts and epiphytes of Micarea and Placynthiella species in 4-weeks-old cultures: (a)
cell packages of InterlumInterlum massjukiae; (c) schematical drawing of
Radiococcus signiensis (the cells are covered with mucilage), the primary photobiont of Placynthiella
icmalea and P. uliginosaTrentepohlia umbrina; (e)
schematical drawing of Pseudochlorella sp., the primary photobiont of Placynthiella dasaea; (f)
schematical drawing of Pseudococcomyxa sp., the primary photobiont of Micarea prasina. Scale
= 20 μm.
143
Epiphytes
A total of 17 species out of 14 genera from two
divisions Chlorophyta and Streptophyta were
(see Table 2). The most frequent of them was
Trebouxia sp., which was found on the surface
of three lichen specimens. The highest number
the surface of Placynthiella dasaea which grew
on decomposed wood (No. 1, 2). In general, the
specimens of Placynthiella had more epiphytes
than Micarea. Trentepohlia annulata, which was
discovered on the surface of the thallus of M.
misella as an epiphyte at , was later found
in the apothecia of the same lichen (Fig 1b).
Fig. 3. Micrographs and schematical drawings of primary photobionts of Micarea species in
4-weeks-old cultures: (a, b) Elliptochloris bilobata, photobiont of Micarea misella and M. prasina; (c,
d) E. subsphaerica, photobiont of M. melanobola, M. prasina and M. subnigrata; (e, f) E. reniformis,
photobiont of M. peliocarpa. Scale = 10 μm.
144 Folia Cryptog. Estonica
DISCUSSION
Primary photobiont
The alga, which was registered in all specimens
of a certain lichen species, and associated with
fungal hyphae, is called here the primary photo-
biont. We declare that the primary photobiont of
Placynthiella icmalea and P. uliginosa is Radio-
coccus signiensis; the primary photobiont of P.
dasaea is Pseudochlorella sp. The obtained data
clarify and add new information to previously
known photobiont diversity for investigated
species. Earlier Gloeocystis sp. (probably, =
Radiococcus Schmidle) (Oxner, 1974), Coccobot-
rys lecideae Warén (Ettl & Gärtner, 1995) and
Chlorella sp. (Rosentreter et al., 2007) have been
reported for Placynthiella uliginosa. Chlorella sp.
was discovered in P. icmalea (Rosentreter et al.,
2007). Unknown green coccoid photobiont up to
12 μm in diameter was reported for P. dasaea
(Tønsberg, 1992).
In Micarea, ten out of eleven investigated
specimens were associated with the primary
photobiont from the genus Elliptochloris. One
specimen of M. prasina contained Pseudococco-
myxa sp. as the primary photobiont. According
to the results of molecular phylogenetic studies
(Beck, 2002), some species of Pseudococcomyxa
are closely related to Elliptochloris bilobata.
(1985), who reported Elliptochloris sp. as the
photobiont of M. prasina
of Elliptochloris reniformis and E. subsphaerica
as lichen photobionts. Earlier these two species
were known as free-living terrestrial algae (Ettl
& Gärtner, 1995; Kostikov et al., 2001). The
photobionts of Micarea species were described
as three types of green algae by Coppins (1983):
micareoid, chlorococcoid and “with protococcoid
-
tobiont of Micarea species is micareoid, which
is most likely, according to its description (Cop-
pins, 1983), referring to Diplosphaera chodatii.
Description of the second type, chlorococcoid,
corresponds to the members of Elliptochloris ge-
nus. The third type of Micarea photobiont having
to the photobiont of Scoliciosporum umbrinum,
which is known as Apatococcus lobatus (Beck,
2002). However, these are only our assumptions
Thus, despite
the fact that Coppins (1983) reported “mica- (1983) reported “mica-
Micarea prasina, which
according to its description cannot be Ellipto-
chloris or Pseudococcomyxa, we revealed just
these algae as the primary photobionts of this
lichen species.
Due to relatively high species diversity of the
photobionts among Micarea and Placynthiella
species, we assume a low selectivity of their
mycobiont toward the algal partner. However,
this issue requires further study using lichen
samples from a wider geographic area.
Additional photobionts
In addition to the primary photobiont, several
investigated Micarea and Placynthiella species
(see Table 2). The number and species compo-
sition of these algae varied. These algae were
revealed to be associated with fungal hyphae
directly inside the lichen thalli, but not on its
surface, therefore, they are considered as the
additional photobionts but not as the epiphytes.
Consequently, our results support the observa-
tions of Tønsberg (1992), who distinguished
such additional algae from the specimens of
Placynthiella dasaea. Unfortunately, the algal
species which Tønsberg (1992) mentioned was
could be a member of Radiococcaceae (e.g. Ra-
diococcus signiensis).
Some of additional algae presented in this
article are the common lichen photobionts.
For instance, the species of Asterochloris and
Trebouxia are well known as obligate photobi-
onts and are associated with more than 55% of
all known lichen species (Voytsekhovich et al.,
2011). In our opinion, Asterochloris cf. excentrica
and Trebouxia cf. incrustata that were discovered
in Placynthiella uliginosa (No. 9) possibly got
there from the thalli of neighbouring Cladonia
foliacea (Huds.) Willd. and Neofuscelia pokornyi
(Zahlbr.) Essl., respectively (see Table 2). It is
known that Neofuscelia species form their thalli
with Trebouxia gigantea (Hildreth & Ahmadjian)
Gärtner (Ahmadjian, 1993) and Trebouxia in-
crustata (Beck, 2002), which are closely related
species according to the molecular phylogenetic
studies (Friedl & Büdel, 2008). The species of
Cladonia are associated with Asterochloris spe-
cies (Piercey-Normore & De Priest, 2001). At the
same time, there is at least one report about
Placynthiella icmalea being a parasite of other
lichens (Fedorenko et al., 2006). Unfortunately,
the authors did not indicate the species of lichen
145
hosts on which P. icmalea parasitized. There-
fore, the presence of Asterochloris sp. inside the
thallus of P. uliginosa (No. 10) can be explained
by the nearby growth of Cladonia coniocraea
(Flörke) Vainio and C. foliacea. However, the
specimens of Micarea (Micarea prasina No. 21
and M. subnigrata), were not associated with the
photobionts of neighbouring lichens (see Table
2). It seems that the entry of the photobiont from
the environment into the thallus has a casual
character.
Elliptochloris bilobata, Leptosira thrombi and
Pseudococcomyxa sp. are the facultative photo-
bionts. It means that these algae exist in both
lichenized and free-living stage. Elliptochloris
bilobata has been reported as the photobiont
of Baeomyces rufus, Catolechia wahlenbergii,
Protothelenella corrosa and P. sphinctrioides
(Tschermak-Woess, 1980, 1985); Leptosira
thrombii is known as the photobiont of Throm-
bium epigaeum (Pers.) Wallr. (Tschermak-Woess,
1953, Schiman, 1961: cit. Tschermak-Woess,
1989), and Pseudococcomyxa is known as the
photobiont of Baeomyces (Pott, 1972, Peveling,
Galun, 1976: cit. Tschermak-Woess, 1989), Li-
chenomphalia (Jaag, 1933; Oberwinkler, 1984),
Peltigera (Jaag, 1933), Solorina and Icmadophila
(Jaag, 1933).
Alternatively Interlum spp., Elliptochloris
subsphaerica and Neocystis sp. are known only
in free-living stage and there are no reports
on these species as lichen bionts. We consider
that the presence of these algal species in the
photobiont layer of investigated lichen thalli is
caused by their free-living populations in the
growing-zone of the lichen. The free-living algae
growing in proximity of a lichen can be enveloped
with the fungal hyphae and gradually become
part of the lichen. Lichens with the facultative
(non-trebouxioid) photobiont use the pool of free-
living algae as the source of their autotrophic
component. For instance, the tropical lichen
Strigula sp. often colonizes the free-living Ceph-
aleuros and uses it as the photobiont (Chapman
& Waters, 2001). In most cases the lichens and
their free-living algal bionts share the same
habitat. Thus, the common terrestrial free-living
algae from the genera Nostoc, Scytonema, Stigo-, Scytonema, Stigo-Scytonema, Stigo-, Stigo-Stigo-
nema, Myrmecia, Diplosphaera and Stichococcus
are common photobionts of terricolous lichens
from the families Collemataceae, Psoraceae, Ste-
reocaulaceae and Verrucariaceae (Tschermak-
Woess, 1989; Voytsekhovich et al., 2011).
Thus, the finding of recently described
lithophilous streptophyte algae Interlum mass� mass-mass-
jukiae and Interlum sp. (Mikhailyuk et al.,
2008) inside lichen thalli was unexpected as the
localities where lichen specimens with Interlum
were collected are new for these algae. This is the
Interlum species, and the second
of Streptophyte in whole, as the lichen photo-
Neocystis
sp. as a lichen photobiont.
Epiphytes
Most of the investigated epiphytic algae are
very common terrestrial algae. The species of
Apatococcus, Bracteacoccus, Parietochloris and
Trentepohlia (Fig 2d) are common in aerophytic
habitats: tree-bark and rocks (Ettl & Gärtner,
1995; Gärtner & Stoyneva, 2003; Mikhailyuk et
al., 2003). Radiococcus signiensis is the epibryo-
phyte (Ettl & Gärtner, 1995). The usual habitat
of Chlamydomonas, Diplosphaera, Interlum,
Leptosira and Pseudococcomyxa is soil, although
they can be found also in aerophytic conditions
(Ettl & Gärtner, 1995; Kostikov et al., 2001;
Mikhailyuk et al., 2008). In contrast, the spe-). In contrast, the spe-. In contrast, the spe-
cies of Trebouxia and Asterochloris are known
only as the obligate photobionts of lichens (Ah-
madjian, 1987). The of epiphytic algae
Trentepohlia in lichen apotecium may indicate
that the algae that grow in the immediate vicinity
of a lichen may be included in its thallus. At the
moment we do not know whether this alga can
be considered as a photobiont, and such cases
require additional investigations.
Lichens
The taxonomical status of Micarea melanobola
which for a long time was considered to be a vari-
ation or synonym of Micarea prasina (Hedlund,
1892; Vězda & Wirth, 1976), is
The species, M. melanobola, was described on
the basis of the differences in thallus and epi-
thecium pigmentation, size of apothecia, spores,
microconidia and the number of paraphyses in
comparison with M. prasina (Coppins, 1983).
Later, these two species were synonymized
because of the absence of distinctions except
pigmentation of apothecia and pycnidia (Czar-
nota, 2007). However, three years later, after
molecular phylogenetic analysis of the lichens
from M. prasina-group, it was noticed that the
dark-colored morphotypes of M. prasina still
required an additional critical investigation
146 Folia Cryptog. Estonica
(Czarnota & Guzow-Krzeminska, 2010). There-uzow-Krzeminska, 2010). There--Krzeminska, 2010). There-Krzeminska, 2010). There-, 2010). There-10). There-). There-There-
fore, the question on the species status of M.
melanobola is still open and any new distinct
features might be useful for its taxonomical
elaboration. We did not reveal any valuable dif-
ferences between the photobiont composition
of M. melanobola and M. prasina. The primary
photobiont of M. melanobola was Elliptochloris
subsphaerica, while different specimens of M.
prasina had E. bilibata, E. subsphaerica and
Pseudococcomyxa sp. as primary photobionts.
We conclude that the photobiont composition
of M. melanobola can not be used as a distinct
A few specimens of Placynthiella uliginosa
were collected from sandstones or soil (No. 3, 6,
11), and several (No. 1, 2, 4, 5, 7, 8, 9, 10) from
mosses and lignum. Micarea prasina is a wide-
spread epiphytic lichen in temperate zone which
is not restricted to any certain phorophytes; our
specimens were collected from Betula, Fraxinus
and Quercus. The specimen of M. misella was
collected from touchwood (decomposed stub),
and M. subnigrata from the thallus of another
lichen. Based on our data, we suggest that the
distribution of studied lichen species does not
depend on the habitat of a certain algal species,
and that the lichen-forming fungi are labile
enough in their photobiont choice. The investi-
gated species of lichen-forming fungi of Micarea
and Placynthiella showed a very low selectivity
to their algal component on the generic level.
Consequently, the species of these lichen genera
are characterized by unstable photobiont com-
bionts. Only two species, Placynthiella uliginosa
and Micarea prasina, showed certain selectiv-
ity to their primary photobionts on the species
level in spite of the presence of some additional
photobionts. In our opinion, such a plasticity
of studied lichen-forming fungi with respect to
their photobionts contributes to their coloniza-
tion of different substrates in different habitats.
ACKNOWLEDGEMENTS
Authors would like to express their gratitude to
the closest colleague Prof. Kondratyuk S. Ya. and
Dr. Mikhailyuk T. I. for their constant discus-
sions and kind support during this work. Also,
acknowledgements are due to Prof. Khodosovt-
sev for valuable comments and provision of some
literature records.
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