The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light

Abstract

Closely related strains of thermophilic Synechococcus were cultivated from the microbial mats found in the effluent channels of Mushroom Spring, Yellowstone National Park (YNP). These strains have identical or nearly identical 16S rRNA sequences but are representative of separate, predicted putative ecotype (PE) populations, which were identified by using the more highly resolving psaA locus and which predominate at different vertical positions within the 1-mm-thick upper-green layer of the mat. Pyrosequencing confirmed that each strain contained a single, predominant psaA genotype. Strains differed in growth rate as a function of irradiance. A strain with a psaA genotype corresponding to a predicted PE that predominates near the mat surface grew fastest at high irradiances, whereas strains with psaA genotypes representative of predominant subsurface populations grew faster at low irradiance and exhibited greater sensitivity to abrupt shifts to high light. The high-light-adapted and low-light-adapted strains also exhibited differences in pigment content and the composition of the photosynthetic apparatus (photosystem ratio) when grown under different light intensities. Cells representative of the different strains had similar morphologies under low-light conditions, but under high-light conditions, cells of low-light-adapted strains became elongated and formed short chains of cells. Collectively, the results presented here are consistent with the hypothesis that closely related, but distinct, ecological species of Synechococcus occupy different light niches in the Mushroom Spring microbial mat and acclimate differently to changing light environments.

RfpA, RfpB, and RfpC are the Master Control Elements of Far-Red Light Photoacclimation (FaRLiP)

“…Soil and fresh-water cyanobacteria encounter FRL because it penetrates more deeply into soils and because plant canopies strongly enrich for FRL because of absorption by chlorophylls (Chl) a and b (Gan and Bryant, 2015). Similar effects occur in microbial mats and sometimes in blooms, where self-shading can provide a powerful selection for alternative, light-harvesting antenna systems (Kühl and Jørgensen, 1994; Nowack et al, 2015; Olsen et al, 2015). We recently discovered two photoacclimation processes that occur in some cyanobacteria in FRL and/or low light, here denoted Far-Red Light Photoacclimation (FaRLiP) (Gan et al, 2014, 2015; Gan and Bryant, 2015) and Low Light Photoacclimation (LoLiP) (Nowack et al, 2015; Olsen et al, 2015).…”

“…Similar effects occur in microbial mats and sometimes in blooms, where self-shading can provide a powerful selection for alternative, light-harvesting antenna systems (Kühl and Jørgensen, 1994; Nowack et al, 2015; Olsen et al, 2015). We recently discovered two photoacclimation processes that occur in some cyanobacteria in FRL and/or low light, here denoted Far-Red Light Photoacclimation (FaRLiP) (Gan et al, 2014, 2015; Gan and Bryant, 2015) and Low Light Photoacclimation (LoLiP) (Nowack et al, 2015; Olsen et al, 2015). During the FaRLiP response, specialized paralogous proteins replace 17 core subunits of the three major photosynthetic complexes: Photosystem (PS) I, PS II, and the phycobilisome.…”

“…in microbial mats associated with Mushroom Spring in Yellowstone National Park. In this acclimation response, cells only synthesize Chl a , but a three-gene operon, apcD4-apcB3-isiX , is expressed that leads to absorption beyond 700 nm, and cells exhibit improved growth at low irradiance (Nowack et al, 2015; Olsen et al, 2015). The apcD4-apcB3-isiX operon does not occur in high-light-adapted ecotypes of Synechococcus sp.…”

Adaptive and acclimative responses of cyanobacteria to far‐red light

“…In particular, the speciation of Synechococcus has been extensively studied with respect to the physicochemical gradients (especially light and temperature) that occur in this system, and putative ecotypes have been identified that are differently distributed as a function of such gradients and that were predicted to have different adaptations to light (Becraft et al ., ; ). Isolates of high‐light‐adapted and low‐light‐adapted putative ecotypes were obtained, and these isolates were characterized with respect to their growth behavior under different irradiance conditions (Nowack et al ., ). These studies showed that low‐light‐adapted ecotypes grow faster at low irradiance but are more sensitive to high light, while high‐light‐adapted isolates tolerate high light much better but are unable to grow as rapidly as low‐light‐adapted isolates at low irradiance.…”

Ecotype Simulation 2: An improved algorithm for efficiently demarcating microbial species from large sequence datasets

“…These PEs were shown to inhabit different locations within the vertical profile of the mat, with PEs B 9, A1, A4, then A14 progressing from the surface to 1 mm below [2]. More recently, Synechococcus isolates that share the same psaA sequence as PEs A1 (strain JA-3-3Ab), A4 (strain 65AY6A5), and A14 (strain 60AY4M2) demonstrated different adaptive and acclimative responses to light intensity and quality, with optimal growth in vitro similar to conditions present where they can be found in the vertical profile of the mat in situ [30]. Comparative genomics and transcriptomics have elucidated genetic differences among these PEs that explain their different metabolic requirements (e.g., low-light adapted PEs were found to have an extra cassette of photosynthetic antenna genes that allow spectral fine tuning under low-light conditions) [34].…”