Gloeocapsopsis aurea, a new subaerophytic cyanobacterium from maritime Antarctica

Polar Biol (2004) 27: 623–628 DOI 10.1007/s00300-004-0620-6

O R I GI N A L P A P E R

Gabriela Mataloni Æ Jirˇ ı´ Koma´rek

Gloeocapsopsis aurea, a new subaerophytic cyanobacterium from maritime Antarctica

Received: 13 November 2003 / Revised: 22 March 2004 / Accepted: 22 March 2004 / Published online: 11 May 2004
Springer-Verlag 2004

Abstract The cyanobacterial flora of maritime Antarctica appears to contain many endemic species and only few cosmopolitan or wider-distributed taxa. Several morphospecies that have been erroneously identified in the past following available keys from temperate or tropical zones belong in fact to little-known and poorly described Antarctic cyanobacteria. Here we describe the taxonomy of one such example, the colonial species Gloeocapsopsis aurea . This cyanobacterium produces irregular, packet-like colonies that form black mats, films and crusts. Based on analysis of algal samples from Punta Cierva (Antarctic Peninsula) and King George Island (South Shetland Islands), this taxon is widely distributed in coastal, deglaciated areas of the maritime Antarctic. It is an important, often dominating, ecotype, mostly colonising irrigated rocks but also found in a variety of other aquatic and semi-aquatic habitats under a wide range of conductivities, pH and nutrient regimes.

Introduction The Antarctic cyanobacterial microflora includes a high number of specialised morpho- and ecotypes, participating in or even dominating algal assemblages in terrestrial and freshwater biotopes in deglaciated areas of maritime coastal regions (West and West 1911; Broady 1981; Ohtani 1986; Pizarro et al. 1996; Koma´rek and Koma´rek 1999, 2003; Mataloni and Pose 2001). G. Mataloni (&) Laboratorio de Limnologı´ a, Facultad de Ciencias Exactas y Naturales, UBA, Pab. II, Ciudad Universitaria, C1428 EHA, Buenos Aires, Argentina E-mail: [email protected] J. Koma´rek (&) Institute of Botany AS CR and Faculty of Biological Sciences, University of South Bohemia, Dukelska´ 135, 37901 Trˇ ebonˇ, Czech Republic E-mail: [email protected]

Numerous types were identified according to traditional keys and monographs, and ascribed to morphologically similar, but ecologically quite different taxa. Many coccoid cyanobacteria growing in packet-like (‘‘sarcinoid’’) clusters belong to this group of misinterpreted species. Several types occur in Antarctic biotopes that can be classified into the modern genera Gloeocapsopsis, Cyanosarcina or to baeocytic Chroococcidiopsis or Myxosarcina. The endolithic Chroococcidiopsis species from arid, continental Antarctica were described mostly by Friedmann and Ocampo (1976), Friedmann (1982) and Friedmann and Ocampo-Friedmann (1984), unfortunately without a final detailed taxonomic analysis. Free-living populations from subaerophytic sites (stones wetted by melted water, seepages, stony surface on edges of temporary creeks, submersed assemblages) were usually ascribed to Myxosarcina burmensis, M. chroococcoides or M. concinna (Parker et al. 1972; Tell et al. 1995; Vinocur and Pizarro 1995), or various Gloeocapsa-species (mainly Gloeocapsopsis magma; Ohtani et al. 1991; Pizarro et al. 1996; Pankow et al. 1987; Ohtani and Kanda 1987), which in turn have been recently reclassified mainly into the genus Gloeocapsopsis (Koma´rek and Anagnostidis 1989). The ecology and also the phenotypic diacritic features of all these species differ from those of Antarctic populations, proving the revision of such morpho- and ecotypes necessary. To such special Antarctic species, commonly distributed along humid maritime Antarctica, belongs our Gloeocapsopsis-type, which cannot be identified according to keys for the cyanobacterial microflora from temperate and tropical regions. Its ecology is very distinct, and it plays an important role as the dominant of some Antarctic algal communites. This species is therefore described as the new taxon, Gloeocapsopsis aurea.

Materials and methods From 1998 to 2003, a number of different freshwater environments were sampled in Cierva Point, Antarctic

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Peninsula (Fig. 1). Some results are part of specific investigations (Izaguirre et al. 2001; Mataloni et al. 2003), while many other observations remain unpublished, as part of a general phycological survey of the area. In all cases, conspicuous films and crusts on the rocks were sampled by scraping the stones with clean brushes and placing in PVC flasks. Temperature, conductivity and pH were measured in-situ with electronic meters. Additional water samples were taken in acidwashed PVC flasks for chemical analyses, filtered through Whatman GF/F filters and stored frozen for transport to Buenos Aires, where concentrations of the main nutrients (PO4-P, NO3-N and NH4-N) were estimated as explained in Izaguirre et al. (2001). Algal samples were observed and drawn using an Olympus CX-30 transmitted light microscope with bright field at ·1,000 magnification, and preserved in 1% formaldehyde. Microphotographs were taken using an Olympus BX-40 with an attached Olympus Camedia digital camera. In King George Island, cyanobacterial assemblages were collected and studied in two periods. During the summer season 1987/1988, deglaciated southern areas of the Fildes Peninsula, Ardley Island and northern coast of Nelson Island were visited. In 1995/1996, the southwest coast of Admiralty Bay was investigated, from Italian Valley in Ezcurra Inlet and the whole vicinity of

Fig. 1 Locations from maritime Antarctica where Gloeocapsopsis aurea was sampled for this study

Polish Antarctic Station ‘‘Henryk Arctowski’’, southwards up to Demay Point (Koma´rek 1999; Koma´rek and Koma´rek 1999, 2003). Cyanobacterial mats, crusts and clusters were collected from soils, stones, rocks and water biotopes. In all cases, main ecological parameters were periodically measured (temperature, pH, conductivity, photosynthetic active radiation). Living samples were observed immediately under LM (Olympus CX 30), documented, and preserved in formaldehyde (±2% final concentration) for detailed study. Part of the material was used for establishing cultures (mineral media ‘‘BG 11’’ and ‘‘Z’’). However, attempts to grow G. aurea in monospecific cultures were unsuccessful.

Results Description The colonies form irregular, packet-like, agglomerated, sarcinoid, microscopic or later forming thin macroscopic, granular, blackish mats or crusts on rocky and stony substrates. Sheaths are sharply delimited, partly (in young colonies) colourless, later slightly lamellated, gold-yellow or rusty yellow-brown to orange, copying the outline of cells or cell clusters, never widened in the spherical envelopes characteristic for typical Gloeocapsa-

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species. Cells spherical to irregular-spherical or semiglobose with pale blue-green or greyish content, sometimes with slightly granulated content, (3.2) 4–9 lm in diameter. Cell division irregular; daughter cells usually produce their own envelopes soon after division; cells sometimes divide in rapid frequency and produce several Fig. 2a–f Gloeocapsopsis aurea. a–c Young colonies; d,e ‘‘icona typica’’ (orig.); f old colony with daughter cells being released;

small cells of irregular size and shape (simple form of baeocyte production?). Reproduction by disintegration of colonies, sometimes solitary cells liberated from sheaths. Single pale blue-green cells without sheaths can occur in young colonies and later in well-developed colonies (Figs. 2, 3).

626 Fig. 3a–h Gloeocapsopsis aurea. a–c Young colonies; d–f typical colonies forming mats and crusts; g,h old disintegrating colonies (orig. photograph)

Distribution and ecology G. aurea is distributed commonly in deglaciated, coastal regions of humid maritime Antarctica. On the Antarctic Peninsula, it has been found in five different locations at Cierva Point, Danco Coast. Distinct populations were abundant there at four sampled environments: granodiorite rocks irrigated by snowmelt near the Primavera Station heliport, meltwater from a glacier forming the headwaters of the oligotrophic Torrente stream, the outflow of hypereutrophic Otero Lake (Othello stream), and various points along the course of hypereutrophic Pingu¨inera stream, which flows through a large gentoo penguin rookery. In the South Shetland Islands, we have found G. aurea at more than 37 separate locations in the area of Admiralty Bay (along the coast from Italian Valley to Demay Peninsula), 9 sites at Fildes Peninsula, 2 in Ardley Island and 3 in northern oases of Nelson Island (occasional collections). This cyanobacterium is commonly subaerophytic, growing on stones continuously irrigated by meltwater during summer, where it forms macroscopic, blackish mats and crusts (Koma´rek and Koma´rek 1999). Its

black colour would be due to the presence of a UVradiation screening compound, such as those described by Vincent (2000) for many cyanobacterial communities adapted to high solar exposures. However, it also occurs among other algae and cyanobacteria on the wet walls of small caves, in seepages (Koma´rek and Koma´rek 2003), on the stony edge of streambeds or as a conspicuous component of the epilithic community at the bottom of small creeks (Mataloni et al. 2003), growing during the Antarctic mid-summer season. Table 1 shows the values of some key environmental parameters for locations of G. aurea at Cierva Point. According to these data, this species grows at a wide range of pH, conductivity and nutrient concentrations and is well adapted to the varying chemical characteristics of meltwaters, from dilute meltwaters of glacial origin to streams draining a gentoo penguin rookery and hypereutrophic Otero Lake. This would allow it to play an important ecological role as a pioneer-oxyphototroph on stones and rocks, where it produces the first organic material for further colonisation. It survives desiccation and freezing during winter, suggesting a K-strategy similar to that exhibited by Phormidium autumnale (sensu lato) as a key species in the colonisation of Ant-

627 Table 1 Physico-chemical characteristics of meltwaters irrigating communities containing Gloeocapsopsis aurea at Cierva Point, Antarctic Peninsula Site

Type of growth

PO4-P (mg l)1)

NO3-N (mg l)1)

NH4-N (mg l)1)

Conductivity (lS cm)1)

pH

Temperature (C)

Sampling season

Helicopter landing site Othello stream Pingu¨inera stream Headwaters of Torrente stream

Crust on wet rocks Epilithon Epilithon Epilithon

12.8

0.04–5.8

0.01–1.42

156

5.27–6.08

0–0.2

2002–2003

1.75–1.88 1.46–8.95 0.1

8.73–9.43 0.6–72.7 0.35

2.53–3.28 0.07–23 0.09

168–214 132–298 10

4.96–5.47 4.39–8.81 6.97

7.2–8.2 0–4.4 0.6

1998 2003 1998

arctic soils (Davey 1988), and is evidently an important cyanobacterial type in maritime Antarctica. Diagnosis Gloeocapsopsis aurea sp. nova Coloniae irregulares, conglomeratae, sarcinoideae, microscopicae, postea macroscopicae et tegetes tenua, granulosa, nigrescentes formantes. Cellulae sphaericae, subsphaericeae, semiglobosae vel irregulares, post divisione ambitu diverso, minores, contentu pallide aerugineo, interdum pallide granuloso, 3.2–9 lm in diameter. Vaginae firmae, pallide lamellosae, not dilatatae, coloratae, aureo-lutescentes, luteo-fuscae vel ferrugineo-brunescentes. Reproductio disintegratione coloniis; divisio cellularum irregularis; cellulae solitariae de vaginis firmis liberantur. Habitatio: Subaerophytice in saxis humidis et inter algas in aquis vadosis; Antarctica maritima. Locus classicus: Cierva Point, Danco Coast, Antarctic Peninsula. Icona typica: Icona nostra 2d,e, 3. Typus: Specimen no. BRNM 1.250 (Museum Brno, Czech Republic).

Fuego (Guarrera and Ferrario 1978) are closer to our new species in both morphology and ecology (Fig. 4). The distinctness and ecological importance of G. aurea make its taxonomic definition necessary. The taxonomic classification of this species into the genus Gloeocapsopsis is supported by the type of cell division and reproductive strategy. It is clearly separated from typical Gloeocapsa-species, from which it differs by the type of cell division and morphology of colonies in vegetative stages. The characteristic spherical and widened envelopes, typical for the genus Gloeocapsa, never occur. Morphologically, our species fits in a cluster of the genera Gloeocapsopsis, Cyanosarcina, and baeocytic Chroococcidiopsis or Myxosarcina. Among these, Cyanosarcina has slightly different structure of colonies and does not produce sheath pigments. The relation to

Discussion G. aurea is described here from natural populations, according to the International Code of Botanical Nomenclature (2000). Attempts to culture it have not been successful, although it is a common species. Molecular and ultrastructural evaluation is important for full characterisation of this distinct cyanobacterial type in the context of the modern cyanobacterial system. No morphological and ecological relations to similar populations from other regions were found (see review of species in Koma´rek and Anagnostidis 1998, pp 274– 281). Among well-described related species, only G. pleurocapsoides has yellowish sheaths. This taxon would be the closest to our populations, from which it differs mainly by cell morphology, life cycles and ecology. However, there has been confusion in the past, since individuals ascribed to this species from Tierra del

Fig. 4 Gloeocapsopsis cf. aurea (sub Gloeocapsa pleurocapsoides) according to Guarrera and Ferrario (1978) from Tierra del Fuego

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baeocytic genera remains unclear, since released smaller cells could be interpreted as baeocyte formation (Figs. 2f, 3h). However, they are not quite typical, and the habit of colonies more closely resembles Gloeocapsopsis. Furthermore, the taxonomic importance of this phenomenon is not yet well-established, and recent molecular analyses indicate that several ‘‘sarcinoid’’ non-baeocytic and baeocytic types could be closely related. This means that several other phenotypic characters (form of cells, cell ultrastructure, structure of colonies) would better express evolutionary relationships than the pattern of cell division. Revision of all these genera is necessary, and will require genetic study of multiple strains isolated from different populations and different habitats. Acknowledgements Part of this work has been carried out through a contract between the University of Buenos Aires and the Instituto Anta´rtico Argentino. Funding was provided by the ANPCyTArgentina (grant BID 802/OC-AR-PICT 04440). In the Czech Republic, the study was supported by the projects of the Grant Agency of the Czech Academy of Sciences, nos K6005114 and A6005002/00. We thank Paul Broady, Warwick Vincent and an anonymous referee for their valuable comments on the original manuscript.

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