In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium Chloroflexus aggregans in a Hot Spring Cyanobacteria-Dominated Microbial Mat

Abstract

Chloroflexus aggregans is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum Chloroflexota (formerly Chloroflexi), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, C. aggregans co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the predominant growth modes of C. aggregans, relative transcription levels of energy metabolism- and CO2 fixation-related genes were studied in Nakabusa Hot Springs microbial mats over a diel cycle and correlated with microscale in situ measurements of O2 and light. Metatranscriptomic analyses indicated two periods with different modes of energy metabolism of C. aggregans: (1) phototrophy around midday and (2) chemotrophy in the early morning hours. During midday, C. aggregans mainly employed photoheterotrophy when the microbial mats were hyperoxic (400–800 µmol L−1 O2). In the early morning hours, relative transcription peaks of genes encoding uptake hydrogenase, key enzymes for carbon fixation, respiratory complexes as well as enzymes for TCA cycle and acetate uptake suggest an aerobic chemomixotrophic lifestyle. This is the first in situ study of the versatile energy metabolism of C. aggregans based on gene transcription patterns. The results provide novel insights into the metabolic flexibility of these filamentous anoxygenic phototrophs that thrive under dynamic environmental conditions.

A New Thermophilic Ene-Reductase from the Filamentous Anoxygenic Phototrophic Bacterium Chloroflexus aggregans

“…Two breakthrough works recently appeared enlarge the knowledge of Chloroflexus aggregans and help in better positioning it in the evolutionary scale toward the appearance of photosynthetic organisms (particularly cyanobacteria, also capable of habitat adaptation and considered the ancestors of chloroplasts). The recent descriptions of its cellular ultrastructure [ 38 ] and transcription pathways related to energy metabolism [ 39 ] highlighted astonishing morphological traits, such as a cytoplasm crowded with proto-organelles, and cycling growth modes relying on a noticeable metabolic plasticity. Likewise, it is expected that the enzymatic equipment of this organism could reveal new, interesting and original functionalities that are worthwhile to be investigated.…”

Editorial for the Special Issue: Advances in the Biology of Phototrophic Bacteria

“…This Special Issue highlights recent advances in these aspects. It includes results specifically on green sulfur bacteria (Chlorobi [3]), heliobacteria (Firmicutes [4]), Chloroflexi [5], Cyanobacteria [6,7] and phototrophic purple bacteria (Proteobacteria [8][9][10][11][12][13]). In addition, phylogenetic studies regarding photosynthesis and osmotic adaptation consider representatives of all of these phyla [14,15].…”

“…This Special Issue includes results on identification and genomic characterization of new isolates [9], the adaptation to specific ecological niches in regard to temperature [6], salinity [14] and pH [4]. It also considers aerobic phototrophic purple bacteria and the relations to oxygen and oxidative stress [8][9][10][11]13] as well as environmental interactions [5,7,12] and syntrophic relations [3].…”

“…The changes between oxic and anoxic conditions as well as between light and dark conditions force these gliding bacteria to move up and down in the mat to meet optimal conditions and to change key metabolic reactions to optimize energy generation under the variable conditions. A particularly detailed study on the adaptation to these dynamic environmental conditions, especially to daily moving gradients in microbial mats, has been performed with Chloroflexus aggregatus by metatranscriptomic and proteomic studies [5], in which the in situ metabolic activity of Chloroflexus aggregans in microbial mats of Nakabusa Hot Springs was analyzed [5]. This study reveals a well-coordinated regulation of key metabolic processes to assure that Cfl.…”

“…This study reveals a well-coordinated regulation of key metabolic processes to assure that Cfl. aggregans uses its metabolic flexibility and capability for both phototrophic and chemotrophic growth to optimize its performance under the varying environmental conditions in its natural habitat [5]. During daytime, light is the main energy source supporting phototrophic growth of Cfl.…”