Responses of a Thermophilic Synechococcus Isolate from the Microbial Mat of Octopus Spring to Light

Abstract

Thermophilic cyanobacteria of the genus Synechococcus are major contributors to photosynthetic carbon fixation in the photic zone of microbial mats in Octopus Spring, Yellowstone National Park. Synechococcus OS-B was characterized with regard to the ability to acclimate to a range of different light irradiances; it grows well at 25 to 200 HL]), we noted several responses that had previously been associated with HL acclimation of cyanobacteria, including cell bleaching, reduced levels of phycobilisomes and chlorophyll, and elevated levels of a specific carotenoid. Synechococcus OS-B synthesizes the carotenoids zeaxanthin and ␤,␤-carotene and a novel myxol-anhydrohexoside. Interestingly, 77-K fluorescence emission spectra suggest that Synechococcus OS-B accumulates very small amounts of photosystem II relative to that of photosystem I. This ratio further decreased at higher growth irradiances, which may reflect potential photodamage following exposure to HL. We also noted that HL caused reduced levels of transcripts encoding phycobilisome components, particularly that for CpcH, a 20.5-kDa rod linker polypeptide. There was enhanced transcript abundance of genes encoding terminal oxidases, superoxide dismutase, tocopherol cyclase, and phytoene desaturase. Genes encoding the photosystem II D1:1 and D1:2 isoforms (psbAI and psbAII/psbAIII, respectively) were also regulated according to the light regimen. The results are discussed in the context of how Synechococcus OS-B may cope with high light irradiances in the high-temperature environment of the microbial mat.Laminated microbial mats are present in the channels emanating from Octopus Spring, an alkaline, siliceous hot spring in Yellowstone National Park (44). Several studies have focused on the community structure (15,32,35) and the physiological/ecological features (34, 44) of the microbial biota of the mat and have helped to elucidate fundamental principles of community ecology and microbial diversity in this environment (2,31,43,44). Recent metagenomic analyses of these consortia are also beginning to reveal ways in which individuals of this community contribute to overall population metabolism (3a). Microbial hot spring communities represent excellent model systems for exploring how environmental parameters, such as light levels, temperature, nutrient availability, and oxic/anoxic conditions, shape the structural and functional aspects of the community. The photic zone of the microbial mat present in Octopus Spring comprises the uppermost 1 to 2 mm. In this region, cyanobacteria, represented by the genus Synechococcus, evolve O 2 and fix inorganic carbon (2). During the day, O 2 levels may reach Ͼ600% air saturation in the photic zone as a consequence of high rates of O 2 evolution and diffusion barriers associated with the polysaccharide matrix of the mat (34). Conversely, as light levels decline in the evening, the O 2 concentration rapidly diminishes and the mat becomes anoxic (34).Recent observations based on denaturing gradient gel electrophoresis and 1...

Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses

“…For instance, closely related Synechococcus 16S rRNA sequences designated A 00 , A 0 , A, B 0 and B, were detected at progressively lower temperatures from about 701C to about 501C, respectively Ward et al, 1998). Furthermore, recent experiments with Synechococcus isolates representing some of these 16S rRNA sequences suggest that they are physiologically adapted to temperature ranges and light intensities experienced in situ (Allewalt et al, 2006;Kilian et al, 2007). There is also evidence of vertical stratification of Synechococcus populations within the microbial mats.…”

“…Because the mat Synechococcus populations have been extensively characterized at the level of rRNA diversity and physiology, and are available as isolates, they provide optimal starting material for high-resolution molecular analyses to establish links between physiological differences, niche partitioning strategies and microbial diversity within the mat community (Steunou et al, 2006;Kilian et al, 2007). Here, we present our approach in which we sequenced the genomes of two isolates of Synechococcus derived from different temperature regions of the mat.…”

Alternative pathways for phosphonate metabolism in thermophilic cyanobacteria from microbial mats

“…These isolates are differentially distributed along the horizontal thermal gradient of the mat. Syn OS-B 0 is prevalent at 53-60 1C whereas Syn OS-A dominates at higher temperatures (58-65 1C) (Allewalt et al, 2006;Kilian et al, 2007). In recent studies we showed that both Syn OS-A and Syn OS-B 0 contain an extensive suite of genes in the Pho regulon, which is required for efficient acquisition of P (Supplementary Table S1).…”

“…Axenic cultures of Syn OS-A (CIW 14) were isolated from original enrichment cultures using the same strategy as described by Kilian et al (2007). Cultures were grown and maintained at 50 1C in liquid D medium supplemented with 10 mM HEPES (4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid (pH 8.2-8.3)) and Va vitamins.…”

Genomics, environmental genomics and the issue of microbial species

“…The mat communities are ideal for such analyses: (i) they have an uneven community structure skewed toward large, predominant type-A/B Synechococcus populations, (ii) genetically and ecologically relevant isolates, both axenic and nonaxenic, of the type-A/B populations are available (Allewalt et al, 2006;Kilian et al, 2007), (iii) the mats have well-defined temperature, light and chemical gradients that can be measured at the microscale level using microsensors that can also quantify photosynthesis and other microbial activities in situ (Ward et al, 2006) (Figure 1), (iv) these gradients can be experimentally subsampled (Ramsing Environmental genomics and microbial species DM Ward et al et al, 2000;Ferris et al, 2003), (v) the mats have very high biomass, are readily accessed, and are protected within Yellowstone National Park, (vi) there is background information on the predominance and distribution of the specific 16S rRNA and ITS genotypes in the mat and (vii) previous studies have explored cyanobacterial physiology over the diel cycle (for example, van der Meer et al, 2005van der Meer et al, , 2007. This strong foundation allows for the development of rational hypotheses related to studies of acclimation and adaptation within and between putative ecotype populations.…”