Freshwater Epiphytic Cyanoprocaryotes from Central Mexico

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Arch. Protistenkd. 143 (1993): 237-247 Fischer Verlag Jena

© by Gustav

FOR

PROTISTEN KUNDE

Freshwater Epiphytic Cyanoprocaryotes from Central Mexico I. Cyanocystis and Xenococcus

GUSTAVO MONTEJANO, MICHELLE GOLD &

JII!:j.f KOMAREK

Universidad Nacional Autonoma de Mexico, Mexico City, Mexico Czech Academy of Sciences, Department of Plant Ecology, Trebori, Czechoslovakia

Summary: Three freshwater, epiphytic species of the cyanoprocaryotic (cyanophycean, cyanobacterial) genera Cyanocystis (C. mexicana spec. nova) and Xenococcus (X. willei GARDNER, X. bicudoi spec. nova), which occur commonly in streaming, unpolluted waters of central Mexico, were studied and documented. The generic diacritical features of Cyanocystis and Xenococcus are discussed. Key Words: Epiphytic Cyanoprocaryotes; Cyanophytes; Cyanobacteria; Cyanocystis; Xenococcus; Taxonomy; Species ecology; Rivers; New species; New descriptions; Mexico.

Introduction

Results

During the investigation of freshwater algal flora of central Mexico rich populations of several epiphytic cyanoprocaryotes were found, which are not well known till now and whose taxonomic position is not definitely solved. Three interesting species from the genera Cyanocystis with nanocytic cell division and Xenococcus with irregular binary fission combined with nanocyte (baeocyte) production are described and documented in this article. The delimitation of both these genera is discussed. The research of freshwater algae in Mexico is organised in the frame of the project of UNAM (Universidad Nacional Autonoma de Mexico). The authors are indebted particularly to the head of this project, Prof. JORGE GONZALEZ GONZALEZ, for the support of their work.

Cyanocystis mexicana spec. nova (Figs. 1- 3) Description: Cells sessile, solitary or gathered in groups, heteropolar, pyriform or widely club-shaped, widely rounded at the apex, narrowed to the base; cell content pale greyish blue-green, homogeneous or later usually with scattered fine granules. Sheath (pseudovagina) thick, colourless, distinct particularly in old cells. Reproduction only by nanocytes; cells divide successively (Fig. lc, arrows; Fig. 2: 14-17) into a large amount of small, spherical nanocytes (Fig. l d), which liberate from the pseudovagina solitary or in clusters by its opening at the cell apex (Fig. 1d; Fig. 2: 11; arrows.

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Cyanoprocaryotes from Central Mexico

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Fig. 2. Cyanocystis mexicana spec. nova: 11 empty sheath (arrow); 14-15 first division of cells, perpendicular to the substrate; 16-17 nanocyte formation.

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Fig. 3. Cyanocystis mexicana spec. nova: sessile groups of cells.

Dimensions: Cells - 45 (50) X - 32 (39) 11m, nanocytes 2.5 - 3.5 (4.5) 11m in diameter. Ecology : Epiphytic on filamentous algae (Co mpsopogo n, Cladophora. Rhizoclonium} and leaves of submerse mosses in clear streams in limestone region of Panuco basin, San Luis Potosi , Mexico.

Locus classicus: small stream flowing to the Rio Tampaon , about 23km SW from Valles (leg. G. MONTEJANO) . Etymology: Species after country of discovery designated .

Cyanoprocaryotes from Central Mexico Diagnosis: Cellulae sessiles, solitariae vel conglomeratae, heteropolares, obovatae vel pyriformes, basim attenuatae, apice rotundatae, contentu pallide griseo-aeruginoso, subtiliter granuloso, ad 50 11m longae et ad 3911m latae. Pseudovagina distincta, firma, incolora. Reproductio nanocytis numerosis sphaericis, 2.5 - 4.5 11m in diametro, de cellula matricali deinceps divisis; nanocyta de pseudovagina ruptura apicali liberantur. - Typus: specimen no. 2620 (in Univ. Autonoma Mexico, seccio phycologica, Mexico City, deposita); iconotypus: figurae nostrae Ie-d. - Habitatio: Epiphytice ad algas filamentosas plantasque in aquis fluentibus in regionibus calcareis; locus classicus: rivulus prope Rio Tampaon, San Luis Potosi, Mexico centralis. This species is similar to freshwater Cyanocystis species with more or less club-shaped cells living in groups (c. pseudococcoides, C. valiae-allorgei, C. aquae-dulcis), from which it differs mainly by coloration or morphology and ecology. However, the mentioned first two species were described from Guadeloupe; C. mexicana proves also the significant diversity of this genus in central America. Xenococcus chroococcoides, described by FRITSCH (1929) from England with similar ecology (epiphytic on Cladophora) is habitually near to C. mexicana, but differs by dimensions and by binary fission in young cells. Several marine Cyanocystis-species correspond morphologically and biologically well with our species. The generic determination is indicated also by the first vertical cell division of mother cells (Fig. 1c, upper arrows).

Xenococcus willei

GARDNER

1927 (Figs. 4-5)

Description: Cells sessile, solitary or in groups, irregular rounded, later spherical or hemispherical, up to reverse droplike with widely rounded apical end and narrowed to the base, heteropolar; cell content bright bluegreen, homogenous, sometimes with solitary dark brown granules (Fig. 4c). Sheath (pseudovagina) distinct, thick, firm, colourless. Cells divide by binary fission, but later often into numerous, small nanocytes, which liberate from sheaths after their apical disintegration (Fig. 4£), and attach again to the substrate, solitary or in groups. Dimensions: cells up to 20 (22) 11m in diameter, nanocytes 2.5 - 3.8 11m in diameter. Sometimes remain 1- 2 nanocytes in emptied sheaths and grow again inside (Fig. 4f, asterisk). Ecology: Epiphytic on filamentous cyanoprocaryotes (Lyngbya cf. majuscula) and submerse algae (Cladophora), mainly in streaming waters. This species was found in several places of central Mexico. The specimens documented in Figs. 4-5 were collected from the creek Quila Mulla, Morelos, central Mexico, from a granitic area, at June 7th 1991, by M. GOLD. Our specimens do not differ substantially from the original description of X. willei from Porto Rico (GARDNER 16 Arch. Protistenkd., Bd. 143, [-3

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1927, our Fig. 4a). This species was found also in thermal waters in Japan and published originally under the name X. schousboei f. thermalis EMOTO et HIROSE and X. willei var. thermalis (EMOTO et HIROSE) EMOTO et HIROSE (HIROSE & HIRANO 1981). This species is probably distributed mainly in clear, continually warm, streaming waters.

Xenococcus bicudoi spec. nova (Figs. 6-7) Description: Cells sessile, more or less hemispherical or slightly flattened, circular or irregular rounded in outline, solitary or gathered one to another, covering sometimes the substrate (mainly filamentous algae) in more or less continual layer; cell content pale, greyish blue-green, homogeneous or finely granular. Sheath thin, colorless, more distinct only during nanocytic division. Cells divide irregularly by binary fission, in different planes perpendicular to the substrate, and, occasionally, by nanocyte formation (Fig. 6); the differences between repeated binary fission and nanocytic division are quantitative and transient. Dimensions: cells (3.5) 4.8 -12.5 11m, nanocytes 3 - 3.5 11m in diameter. Ecology: Epiphytic on submerse filamentous algae (mainly Cladophora) in not polluted, usually neutral or slightly alkalic and mineralized rivers with summer temperature more or less over 20°C, sometimes to the depth more than 60cm. Known from several localities in central Mexico, usually from mountains (San Luis Potosi, Tamasopo, Agua Buena - leg. G. MONTEJANO, 1985; Morelos, Rio Itzamatitlan, Cocoyoc - leg. M. GOLD, 1992; Puebla, San Antonio, Texcala - leg. E. NOVELO, 1991). Diagnosis: Cellulae sessiles, plus minusve hemispharicae, solitariae vel irregulariter conglomeratae, paucim applanatae, contentu pallide griseo-aeruginoso, homogeneo vel subtiliter granuloso, 3.5 - 12.5 11m in diametro. Pseudovagina tenuis, incolora, firma, distincta ad cellulis adultis. Divisio cellularum in partes duas, irregulariter in planis diversis ad substratum perpendicularibus, vel in nanocyta numerosa, sphaerica, 3 - 3.5 11m in diametro; nanocyta ruptura apicali pseudovaginae liberantur. - Typus (iconotypus): figura nostra 6. - Habitatio: Epiphytice ad algas filamentosas in aquis fluentibus Americae tropicalis subtropicalisque, praecipue in montibus; locus classicus: rivulus Agua Buena prope Tamasopo, Mexico centralis. - Etymologia: Species ad honorem profess. CARLOS BICUDO, Sao Paulo, Brasilia, nominata.

X. bicudoi, which corresponds well with the generic diagnosis of Xenococcus and morphologically is similar to the type species, X. schousboei, seems to be common at corresponding localities in central Mexico and possibly over the whole central and tropical America. It is prob-

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Fig. 4. Xenococcus willei G ARDNER : a iconotype after G ARDNER 1927; b after E MOTO et HIROSE from Japan ; c- e solitary cells and their groups; f small groups of cells with dividing cells (nanocyte formation) and empty sheaths (asterisks = growth of nanocytes within the empty sheath). Orig.

Cya noprocaryotes from Central Mexico

Fig. S. Kenococcus willei central Mexico.

GARDN ER :

solitary cells and their groups attached to filaments of Lyngbya cf. majuscula from

able , e . g., that "X . schousboei var . pal/ida ", which was selected as an example of Xenococcus among "A lgae of continent al waters of Brasilia" by BICUDO & BICUDO (19 70) co uld be identical also with this species (the ori16*

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ginal X. schousboei is an ecologicall y very limited marine littoral spec ies, which occurs , e .g ., in intertidal zone of Atlantic coas t and its occurrence in streaming waters of tropi cal Ame rica is impossi ble.)

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a

r

Fig. 6. Xenococcus bicudoi spec. nova: a small groups of cells with few dividing cells by binary fission; b-c cells growing in groups on filamentous algae ; d small groups of cells, arrow indicate the nanocyte formation. Orig.

Discussion The spec ies from the complex of cyanoprocaryotic genera Dermocarpa-Dermocarpella-Cyanocystis-Xenococcus are little known and also their delimitation on the generic level is not satisfactory solved. As was shown (GINSBURG-ARDRE 1966; FELDMANN & FELDMANN 1953 ; BOURRELLY 1970; WATERBURY & STANIER 1978), the

type material (exsiccate, original drawing , description) of the genu s Dermocarpa represents a mixture of species and enabl es different explanations of generic concepts. Becau se this whole genu s was entirely confused and not typifiable (the different authors selected different parts of the type material for the later typification; KOMAREK & ANAGNOSTIDIS 1986), GEITLER (1967) proposed to eliminate the name "Dermo carpa " entirely according to the

Cyanoprocaryotes from Central Mexico

Fig. 7. Xenococcus bicudoi spec. nova: groups of cells on filamentous substrates. 17

Arch. Protistenkd., Bd. 143, 1-3

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Art. 69 and 70 of Botanical Code. BOURRELLY (1970) precised particularly the generic concept of Cyanocystis, which is the correct name of the majority of species, originally classified as "Dermocarpa", For classification of the rest of species in question (from the genera Dermocarpella, Xenococcus, etc.) on the generic level, it is necessary to compare them with the type species of other genera and to use the modem knowledge about the biology of different taxa. In principal, there exist four groups of genera, which differ in reproduction strategy and can be classified into the different families: (i) The cells divide exclusively by multiple fission into nanocytes, successively or spontaneously; they grow in solitary cells or in their clusters and are usually polarized, attached by one end (or by one side) to the substrate (fam. Dermocarpellaceae; incl. Dermocarpella and Cyanocystis). (ii) The cells divide exclusively by irregular binary fission (in different planes or sometimes, predominantly, in one plane), forming pseudoparenchymatous strata on the substrate; on the margin of colonies arise sometimes short radiating and irregular pseudofilaments (fam. Hydrococcaceae) . (iii) The cells divide repeatedly by binary fission or, alternatively, by multiple fission; the cells grow freely aggregated in irregular, subspherical clusters or in colonies, attached to the substrate (fam. Xenococcaceae). (iv) The cells divide commonly by binary fission and form pseudoparenchymatous or pseudofilamentous thalli, but in special parts of a thallus the cells divide by multiple fission into nanocytes (baeocytes); pseudofilaments are sometimes shortened or branched (fam. Hyellaceae). Our Cyanocystis mexicana belongs evidently into the genus Cyanocystis. The cells never divide by binary fission, but successively into the large amount of small nanocytes (Fig. 1d; Fig. 2: 17). They liberate from splitted sheaths (pseudovaginae, Fig. l d, upper arrow) in clusters, which attach again to the substrate. The first cell division is perpendicular to the substrate (Fig. 1c, upper arrows; Fig. 2: 14-15, arrow). The growth of cells seems to be not synchronized; cells of different size occur usually in one group of cells. The present Xenococcus THUR. in BORN. et THUR. 1880, which is the type genus of the family Xenococcaceae, should be therefore characterized by sessile cells, which are able to divide during the vegetation by binary fission and occasionally by successive (succedan) multiple fission into the nanocytes (baeocytes). This type of life cycle is characteristical for the whole family, comprising the free living genera Chroococcopsis, Chroococcidiopsis and others, or the sessile Xenococcus. In fact, the present genus Xenococcus is heterogeneous and with its diagnosis based on the type species X. schousboei

(marine species) correspond only several other taxa (freshwater X. kerneri, marine X. chaetomorphae, X. cladophorae, etc.): our X. bicudoi belongs to this group as well. The rest of Xenococcus taxa comprises two distinct groups, differing from the Xenococcus (and the Xenococcaceae) diagnosis: 1. Species with very fine, minute cells, forming the dense , unicellular layer on the substrate; the cells are slightly elongated (from aside) and in principle polarized, attached by one end to the substrate. To this group belong freshwater species (X. rivularis, X. gracilis, X. minimus), or marine species (X. laysanensis). In these types never the nanocyte formation was found, and the cell division is not well known. Because the cells are sometimes very densely, parallely agglomerated and from above possess the more or less polygonal outline, the irregular binary fission (perpendicular to the substrate) is supposed. However, several of these types can grow in two layers (X. minimus var. starmachii), and therefore also the fission perpendicular to the vertical axis must occur. In this case, the difference from some chamaesiphonacean species is negligible, and all these types are very near, e.g., to Chamaesiphon investiens SKUJA 1964 or Ch.regularis (FRITSCH) GEITL. 1929. The unclear generic position follows also from the fact, that several previous authors classify these types in special genera (HANSGIRG 1889 described originally Xenococcus rivularis as "Cyanoderma", FRITSCH 1929 included his Xenococcus brittanicus = Chamaesiphon regularis into the genus Chamaesiphonopsis, etc.). From the present data available follows , that the whole group is nearest to Chamaesiphon (the cells divide also perpendicularly to the vertical axis of cells) and should be classified as one subgenus of Chamaesiphon or as a special genus of chamaesiphonoid cyanoprocaryotes (Chamaesiphonopsis FRITSCH 1929). In Mexican samples also populations of this character occur which will be discussed in detail in a further study. 2. In the second group, the cells are usually polarized, sometimes pyriform or club-shaped, or gathered into irregular, more or less hemispherical colonies with densely and more or less parallely and vertically arranged cells, flattened at the touching sides. From about 6 described Xenococcus-species of this type, three are known from freshwater biotopes and usually sessile on filamentous algae or mosses. They divide by binary fission and occasionally successively into a great amount of nanocytes. The nanocytes liberate from the mother sheath (pseudovagina) by its gelatinization or by a more or less apical opening (the both ways are usually alternative in one population) and they attach solitary or in clusters (agglomerations, joined by slime together) again to the substrate. By this feature, such species (freshwater X. willei, marine X. pyriforme) are similar to the genus Cyanocystis, as revised by BOURRELLY (1970), from

Cyanoprocaryotes from Central Mexico

which they differ by the initial stage of binary fission of sessile cells . In maj ority of such populations , the first divi sion plane in mother cells is vertical, what is also the characteristical feature of Cyanocystis (comp . C. minima in GEITLER 1932, C. pseudoxenococcoides in BOURRELLY 1970). We cla ssify these types (including X. willei) still as Xenococcus species , but their relation to typical Xenococcus or to the Cyano cystis is not quite clear. Th e whole content of the genus Xenococcus is therefore not precisely defined and practically each species needs further investigation and furth er data about their vari ability, cell and life cycles, ecology and distribution . From the genera Cyan ocystis and Dermocarpella (sooner Dermocarpa p .p.) and the whole family Dermocarpellaceae differs Xenococcus by the cell and life cycle s . The heteropolar dermoc arpellacean cells div ide onl y by multiple fiss ion , i.e., the production of nan ocytes is their onl y mode of repr oduction .

References BICUDO , C . E. M. & BICUDO , R. M. T . (1970): Algas de aguas continentais Brasileiras. Sao Paulo. BOURRELLY , P. (1970): Les algues d 'e au douce . III. Paris. - (1972): Note sur les genres Pleurocapsa et Scopulonema. In: DESIKACHARY, T. V. (ed.) , Taxonomy and Biology of Blue-green Algae , pp. 38-40. Madras . - & MANGUIN, E. (1952): Algue s d'eau douce de la Guadeloupe et dependan ces. Paris. DROUET, F. & DAILY, W . A. (1956) : Revision of the coccoid Myxophyceae. Butler Univ . Bot. Stud. 12: 1-218 . FELDMANN, J. & FELDMANN , G. (1953): Observations sur les genres Dermocarpa et Dermocarpella (Cyanophyceae). Osterr. bot. Ztschr. 100 (4/5): 505-514.

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FRITSCH , F. E. (1929): The encrusting algal communities of certai n fast-flow ing streams. New Phyto!. 28 : 165-196. GARDNER, N. L. (1918): New Pacific coast marine algae III. Univ. Calif . Pub!. Bot. 6 : 455-486. - (1927): New Myxophyceae from Porto Rico . Mem . N. Y. Bot. Garden 7: 1-144 . GEITLER, L. (1932): Cyanophyceae . Rabenhorst' s Kryptogamenflora 14, Leipz ig. - (1942): Schizoph yta (Klasse Schizoph yceae). In: ENGLER & PRANTL , Nat. Planzenfam . lb. - (1967): Entwicklungsgeschichtliche und systematische Untersuchungen in einigen Cyanophyceen. Nova Hedwigia 13 (3/4): 403-421 . GINSBURG-ARDRE, F. (1966): Dermocarpa, Xenococcus, Dermocarpella (Cyanophycees): Nouvelles observation s. Osterr. bot. Ztschr. 113 : 362- 367. HIROSE , H . & HIRANO, M. (1981): Class Cyanophyceae. In: HIROSE , H . & YAMAGISHI , T. (eds.), Illustration s of the Japanese freshwater Algae, pp. 1- 151. Tokyo. KOMAREK , J. & ANAGNOSTIDIS, K. (1986): Modem approach to the classificat ion system of Cyanophytes 2 - Chroococcales, Arch. Hydrobiol./Algo!. Stud . 43 : 157- 226. SETCHELL, W . A . & GARDNER , N. L. (1919): The marine algae of the Pacific coast of North America . 1. Myxophyceae . Univ. Calif. Pub!. Bot. 8 (1) : 1-138 . WATERBURY, J. & STA NIER , R. Y. (1978) : Pattern s of growth and development in pleuroc apsalean Cyanob acteria . Microbio!' Rev. 42 : 2- 44. Received : August 18, 1992 Authors' addresses: Dr. GUSTAVO MONTEJANO , Dr . MICHELLE GOLD, Universidad Nacional Autonoma de Mexico, Laboratorio de Ficologia, A.P. 70-620 , C. U. Coyoacan, 04510, Mexico City, Mexico; Dr. JIIH KOMAREK, Czech Academ y of Sciences, Department of Plant Ecology, Dukelska 145, 37982 Tfebori, Czech Republic .