Ecomorphological Variability of Arthrospira Fusiformis (Cyanoprokaryota) in African Soda Lakes

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Ecomorphological Variability of Arthrospira Fusiformis (Cyanoprokaryota) in African Soda Lakes ORIGINAL RESEARCH Ecomorphological variability of Arthrospira fusiformis (Cyanoprokaryota) in African soda lakes Mary Nakabungo Kaggwa1, Alfred Burian2, Steve Omondi Oduor3 & Michael Schagerl1 1Department of Limnology and Oceanography, University of Vienna, Althanstrasse 14, A-1190 Vienna, Austria 2Department of Ecology, Environment and Plant Sciences, Stockholm University, Frescati Backe, Svante Arrhenius V 21A, SE-106 91 Stockholm, Sweden 3Department of Biological Sciences, Egerton University, P.O Box 536, Egerton, Kenya Keywords Abstract Arthrospira, cell, environment, filament, phytoplankton morphology, saline lakes, The filamentous spirally coiled cyanoprokaryote Arthrospira fusiformis is found Spirulina. in extremely high densities in tropical soda lakes acting as driving force of the food web. We studied pronounced temporal morphological changes of Arthro- Correspondence spira in Kenyan soda lakes, Nakuru and Bogoria, and identified underlying key Michael Schagerl, Department of Limnology factors. Cell (diameter and height) and filament (height of coil, coil diameter, and Oceanography, University of Vienna, and number) dimensions were measured from weekly samples collected over a Althanstrasse 14, A-1090 Vienna, Austria. period of 16 months. In both lakes, medium-sized cells and large, widely coiled Tel: +43 1 4277 76414; Fax: +43 1 4277 876414; E-mail: michael. filaments prevailed most. Percentage of large, widely coiled filaments was pro- [email protected] moted by elevated levels of soluble reactive phosphorus, wind speed, tempera- ture and conductivity and the opposite for small filaments. Large, narrow- Funding Information coiled filaments were associated with an increase in mainly Arthrospira-grazing The financial support offered by the Austrian zooplankton and cyanophage infections. Widely coiled spirals were promoted Partnership Programme in Higher Education by increased turbulences. Based on fluorescence measurements, we found and Research for Development (APPEAR) is highly appreciated. This study was funded by widely coiled filaments representing high vitality. From this study we were able the Austrian Science Fund Project No. to demonstrate for the first time morphological patterns of Arthrospira in nat- P19911 “Factors controlling abundance of ure. Arthrospira morphotypes are suitable for indicating the biological status in A. fusiformis”. soda lakes as they are subjective and therefore reflective of what is happening in its habitat. Additionally, this outcome might be also of interest for commer- Received: 27 May 2013; Revised: 18 July cial ′Spirulina′ farms in enhancing high-quality production. 2013; Accepted: 29 July 2013 MicrobiologyOpen 2013; 2(5): 881–891 doi: 10.1002/mbo3.125 Introduction et al. 2007). It follows therefore that morphological traits adapted by phytoplankton are a reflection of changes and Effective resource exploitation under variable environ- regularities of seasonal and/or environmental patterns. mental conditions is one of the most important causes of They not only show regular periodicities in weather intra- and interspecific morphological diversity in phyto- patterns, but also reflect effects of perturbations or other plankton (Naselli-Flores and Barone 2000; Naselli-Flores disturbances in ecosystem (Naselli-Flores et al. 2007). et al. 2007). Available literature on morphological vari- Arthrospira fusiformis (Voronichin) Komarek and Lund ability of phytoplankton indicates that environmental and is a filamentous cyanobacterium that forms almost unialgal biological constraints such as nutrients, light availability, blooms in soda lakes of the East African Rift Valley (Vare- and grazing pressure from herbivores influence phyto- schi 1978). These lakes are characterized by high levels of plankton morphology (Kagami and Urabe 2001; O’Farrell carbonate and bicarbonate contents and a pH of up to 11 ª 2013 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. 881 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Morphology Changes of Arthrospira M. N. Kaggwa et al. (Vonshak 1997; Oduor and Schagerl 2007a). A. In the shallow African saline–alkaline lakes, it has fusiformis is the main food source of the Lesser Flamingos, already been observed that there are large temporal Phoeniconaias minor Saint-Hilaire (Vareschi and Vareschi fluctuations in A. fusiformis biomass (Oduor and Schag- 1984) linking Arthrospira abundance directly to the high erl 2007a; Schagerl and Oduor 2008; Krienitz and Kotut number of these birds in African saline–alkaline lakes 2010). Even though such shifts in A. fusiformis biomass (Krienitz and Kotut 2010; Kaggwa et al. 2013). Lesser may go along with morphological changes, no compre- Flamingos are a big tourist attraction in Lakes Nakuru and hensive field study has been done on the morphological Bogoria in Kenya, which has economic importance for local variability of A. fusiformis so far. In this study, we people (Harper et al. 2003; Schagerl and Oduor 2008; sought to address this gap by assessing the temporal Krienitz and Kotut 2010). At times, the dominance of morphological changes of A. fusiformis and identifying A. fusiformis suddenly crashes and the lake shifts toward an key environmental and biological variables that were unstable pelagic community of different organisms, which responsible for these changes. Such shifts in morphol- cause high degrees of food insecurity for top-level con- ogy of the dominant primary producer probably have sumers like fish and flamingos (Krienitz and Kotut 2010; significant impacts on the food web structure, as Krienitz et al. 2013). A. fusiformis is commercially sold as grazing might be promoted or hindered by certain “Spirulina platensis” for dietary supplement because of its morphological features. Additionally, the study allowed high content of essential fatty acids, vitamins, proteins, and evaluating the potential of A. fusiformis morphology as minerals (Jassby 1988; Tokusßogulu and Unal€ 2003; a reliable indicator of the biological stability in soda Muhling€ et al. 2005; Zielinska~ and Chojnacka 2009). lakes. Arthrospira fusiformis strains have been observed to occur in a varied range of saline habitats which shows its ability to Material and Methods adapt to freshwater alkaline conditions as well as saline– alkaline and even hypersaline environments (Dadheech Study site et al. 2010). In both natural and culture conditions, it shows high morphological variability (Muhling€ et al. 2003; Ballot This study was carried out in the two Kenyan Rift Valley et al. 2004; Wang and Zhao 2005). The main morphological lakes Nakuru and Bogoria (Fig. 1), which are known to feature of A. fusiformis is the patterned arrangement of its host huge flocks of Lesser Flamingos with numbers some- multicellular cylindrical trichome in an open helix. Tric- times rising over 2 million birds (Vareschi 1978), which homes are composed of cylindrical cells that undergo binary is equivalent to 75% of its world population. fission in a single plane, perpendicular to the main axis. Cell The sampling point in L. Nakuru is located in the cen- diameter ranges from about 3–12 lm, though occasionally tral part at 00°21.387′S, 036°05.519′E which is representa- it may reach up to 16 lm. The helix pitch typically ranges tive of the whole ecosystem due to its polymictic from 10–70 lm and its diameter from 20–100 lm. These character and the small size of the lake (Oduor and two parameters which define the shape of the helix architec- Schagerl 2007b). In L. Bogoria, the sampling point is ture are highly dependent on growth and environmental located at 00°16.166′N, 036°05.766′E in the central region conditions (Vonshak and Tomaselli 2000). of the lake and is one of the deeper parts of the whole Under laboratory conditions, Kebede (1997) detected lake; it gives a good representation of the physical and differences in the length of its trichomes and degree of chemical conditions when compared to the shallower helicity when cultured at varying salinity levels expressing northern and southern parts of the lake. the physiological stress to which the cells were subjected to. The author observed that long trichomes occurred at À Sample collection the lowest salinity level (13 g L 1) while very short but À closely coiled trichomes were dominating in Cl rich and Weather stations with complete data loggers of the À highly saline media (55–68 g L 1). Additionally, very HOBO RG3-M were installed at the shores of both lakes 2À loose helices were distinctive for cultures grown in SO4 (Onset Computer Corporation, USA). Data were logged rich media. The helix feature in A. fusiformis shows high for wind speed, solar radiation, air temperature, and pre- variability (Muhling€ et al. 2003; Wang and Zhao 2005) cipitation. All limnological parameters were sampled which probably is determined at the genetic level and weekly from July 2008 to October 2009 (n = 130 sam- induced by various environmental factors, hence the con- pling occasions). Measurements of environmental in situ cept of ‘plasticity genes’ (Schlichting and Pigliucci 1993). parameters included light attenuation (PAR, Skye instru- This refers to the regulatory loci that directly respond to ments, UK), pH, electrical conductivity, and water tem- a specific environmental stimulus by triggering a specific perature (multiprobe WTW Multi 340i, Wissenschaftlich series of morphogenic changes
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