scholarly journals Carotenoid biomarkers in Namibian shelf sediments: Anoxygenic photosynthesis during sulfide eruptions in the Benguela Upwelling System

2021 ◽  
Vol 118 (29) ◽  
pp. e2106040118
Author(s):  
Jian Ma ◽  
Katherine L. French ◽  
Xingqian Cui ◽  
Donald A. Bryant ◽  
Roger E. Summons

Aromatic carotenoid-derived hydrocarbon biomarkers are ubiquitous in ancient sediments and oils and are typically attributed to anoxygenic phototrophic green sulfur bacteria (GSB) and purple sulfur bacteria (PSB). These biomarkers serve as proxies for the environmental growth requirements of PSB and GSB, namely euxinic waters extending into the photic zone. Until now, prevailing models for environments supporting anoxygenic phototrophs include microbial mats, restricted basins and fjords with deep chemoclines, and meromictic lakes with shallow chemoclines. However, carotenoids have been reported in ancient open marine settings for which there currently are no known modern analogs that host GSB and PSB. The Benguela Upwelling System offshore Namibia, known for exceptionally high primary productivity, is prone to recurrent toxic gas eruptions whereupon hydrogen sulfide emanates from sediments into the overlying water column. These events, visible in satellite imagery as water masses clouded with elemental sulfur, suggest that the Benguela Upwelling System may be capable of supporting GSB and PSB. Here, we compare distributions of biomarkers in the free and sulfur-bound organic matter of Namibian shelf sediments. Numerous compounds—including acyclic isoprenoids, steranes, triterpanes, and carotenoids—were released from the polar lipid fractions upon Raney nickel desulfurization. The prevalence of isorenieratane and β-isorenieratane in sampling stations along the shelf verified anoxygenic photosynthesis by low-light-adapted, brown-colored GSB in this open marine setting. Renierapurpurane was also present in the sulfur-bound carotenoids and was typically accompanied by lower abundances of renieratane and β-renierapurpurane, thereby identifying cyanobacteria as an additional aromatic carotenoid source.

2019 ◽  
Author(s):  
Srijak Bhatnagar ◽  
Elise S. Cowley ◽  
Sebastian H. Kopf ◽  
Sherlynette Pérez Castro ◽  
Sean Kearney ◽  
...  

AbstractPhototrophic microbial mats commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. Here we show that similar coexistence patterns and ecological niches can occur in suspended phototrophic blooms of an organic-rich estuary. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophicCyanobacteria, the middle and lower parts were dominated by anoxygenic purple sulfur bacteria (Chromatiales) and green sulfur bacteria (Chlorobiales), respectively. We found multiple uncultured phototrophic lineages and present metagenome-assembled genomes of two uncultured organisms within theChlorobiales. Apparently, thoseChlorobialespopulations were affected byMicroviridaeviruses. We suggest a sulfur cycle within the bloom in which elemental sulfur produced by phototrophs is reduced to sulfide byDesulfuromonas sp. These findings improve our understanding of the ecology and ecophysiology of phototrophic blooms and their impact on biogeochemical cycles.


2019 ◽  
Author(s):  
Petra Pjevac ◽  
Stefan Dyksma ◽  
Tobias Goldhammer ◽  
Izabela Mujakić ◽  
Michal Koblížek ◽  
...  

AbstractSulfide-driven anoxygenic photosynthesis is an ancient microbial metabolism that contributes significantly to inorganic carbon fixation in stratified, sulfidic water bodies. Methods commonly applied to quantify inorganic carbon fixation by anoxygenic phototrophs, however, cannot resolve the contributions of distinct microbial populations to the overall process. We implemented a straightforward workflow, consisting of radioisotope labeling and flow cytometric cell sorting based on the distinct autofluorescence of bacterial photo pigments, to discriminate and quantify contributions of co-occurring anoxygenic phototrophic populations toin situinorganic carbon fixation in environmental samples. This allowed us to assign 89.3 ±7.6% of daytime inorganic carbon fixation by anoxygenic phototrophs in Lake Rogoznica (Croatia) to an abundant chemocline-dwelling population of green sulfur bacteria (dominated byChlorobium phaeobacteroides), whereas the co-occurring purple sulfur bacteria (Halochromatiumsp.) contributed only 1.8 ±1.4%. Furthermore, we obtained two metagenome assembled genomes of green sulfur bacteria and one of a purple sulfur bacterium which provides the first genomic insights into the genusHalochromatium, confirming its high metabolic flexibility and physiological potential for mixo-and heterotrophic growth.


2013 ◽  
Vol 79 (8) ◽  
pp. 2596-2604 ◽  
Author(s):  
Ekaterina N. Boldareva-Nuianzina ◽  
Zuzana Bláhová ◽  
Roman Sobotka ◽  
Michal Koblížek

ABSTRACTMagnesium-protoporphyrin IX monomethylester cyclase is one of the key enzymes of the bacteriochlorophyll biosynthesis pathway. There exist two fundamentally different forms of this enzyme. The oxygen-dependent form, encoded by the geneacsF, catalyzes the formation of the bacteriochlorophyll fifth ring using oxygen, whereas the oxygen-independent form encoded by the genebchEutilizes an oxygen atom extracted from water. The presence ofacsFandbchEgenes was surveyed in various phototrophicProteobacteriausing the available genomic data and newly designed degenerated primers. It was found that while the majority of purple nonsulfur bacteria contained both forms of the cyclase, the purple sulfur bacteria contained only the oxygen-independent form. All tested species of aerobic anoxygenic phototrophs containedacsFgenes, but some of them also retained thebchEgene. In contrast tobchEphylogeny, theacsFphylogeny was in good agreement with 16S inferred phylogeny. Moreover, the survey of the genome data documented that theacsFgene occupies a conserved position inside the photosynthesis gene cluster, whereas thebchElocation in the genome varied largely between the species. This suggests that the oxygen-dependent cyclase was recruited by purple phototrophic bacteria very early during their evolution. The primary sequence and immunochemical similarity with its cyanobacterial counterparts suggests thatacsFmay have been acquired byProteobacteriavia horizontal gene transfer from cyanobacteria. The acquisition of the gene allowed purple nonsulfur phototrophic bacteria to proliferate in the mildly oxygenated conditions of the Proterozoic era.


2006 ◽  
Vol 188 (17) ◽  
pp. 6217-6223 ◽  
Author(s):  
Julia A. Maresca ◽  
Donald A. Bryant

ABSTRACT The green sulfur bacterium Chlorobium tepidum produces chlorobactene as its primary carotenoid. Small amounts of chlorobactene are hydroxylated by the enzyme CrtC and then glucosylated and acylated to produce chlorobactene glucoside laurate. The genes encoding the enzymes responsible for these modifications of chlorobactene, CT1987, and CT0967, have been identified by comparative genomics, and these genes were insertionally inactivated in C. tepidum to verify their predicted function. The gene encoding chlorobactene glucosyltransferase (CT1987) has been named cruC, and the gene encoding chlorobactene lauroyltransferase (CT0967) has been named cruD. Homologs of these genes are found in the genomes of all sequenced green sulfur bacteria and filamentous anoxygenic phototrophs as well as in the genomes of several nonphotosynthetic bacteria that produce similarly modified carotenoids. The other bacteria in which these genes are found are not closely related to green sulfur bacteria or to one another. This suggests that the ability to synthesize modified carotenoids has been a frequently transferred trait.


2005 ◽  
Vol 71 (7) ◽  
pp. 3544-3550 ◽  
Author(s):  
Mauro Tonolla ◽  
Raffaele Peduzzi ◽  
Dittmar Hahn

ABSTRACT Population analyses in water samples obtained from the chemocline of crenogenic, meromictic Lake Cadagno, Switzerland, in October for the years 1994 to 2003 were studied using in situ hybridization with specific probes. During this 10-year period, large shifts in abundance between purple and green sulfur bacteria and among different populations were obtained. Purple sulfur bacteria were the numerically most prominent phototrophic sulfur bacteria in samples obtained from 1994 to 2001, when they represented between 70 and 95% of the phototrophic sulfur bacteria. All populations of purple sulfur bacteria showed large fluctuations in time with populations belonging to the genus Lamprocystis being numerically much more important than those of the genera Chromatium and Thiocystis. Green sulfur bacteria were initially represented by Chlorobium phaeobacteroides but were replaced by Chlorobium clathratiforme by the end of the study. C. clathratiforme was the only green sulfur bacterium detected during the last 2 years of the analysis, when a shift in dominance from purple sulfur bacteria to green sulfur bacteria was observed in the chemocline. At this time, numbers of purple sulfur bacteria had decreased and those of green sulfur bacteria increased by about 1 order of magnitude and C. clathratiforme represented about 95% of the phototrophic sulfur bacteria. This major change in community structure in the chemocline was accompanied by changes in profiles of turbidity and photosynthetically available radiation, as well as for sulfide concentrations and light intensity. Overall, these findings suggest that a disruption of the chemocline in 2000 may have altered environmental niches and populations in subsequent years.


2021 ◽  
Author(s):  
LM Ward ◽  
PM Shih

AbstractWhile most productivity on the surface of the Earth today is fueled by oxygenic photosynthesis, during the early parts of Earth history it is thought that anoxygenic photosynthesis—using compounds like ferrous iron or sulfide as electron donors—drove most global carbon fixation. Anoxygenic photosynthesis is still performed by diverse bacteria in niche environments today. Of these, the Chlorobi (formerly green sulfur bacteria) are often interpreted as being particularly ancient and are frequently proposed to have fueled the biosphere early in Earth history before the rise of oxygenic photosynthesis. Here, we perform comparative genomic, phylogenetic, and molecular clock analyses to determine the antiquity of the Chlorobi and their characteristic phenotypes. We show that contrary to common assumptions, the Chlorobi clade is relatively young, with anoxygenic phototrophy, carbon fixation via the rTCA pathway, and iron oxidation all significantly postdating the rise of oxygen ~2.3 billion years ago. The Chlorobi therefore could not have fueled the Archean biosphere, but instead represent a relatively young radiation of organisms which likely acquired the capacity for anoxygenic photosynthesis and other traits via horizontal gene transfer sometime after the evolution of oxygenic Cyanobacteria.


2003 ◽  
Vol 69 (7) ◽  
pp. 3739-3750 ◽  
Author(s):  
Jens Glaeser ◽  
Jörg Overmann

ABSTRACT A dense population of the phototrophic consortium “Pelochromatium roseum” was investigated in the chemocline of a temperate holomictic lake (Lake Dagow, Brandenburg, Germany). Fluorescence in situ hybridization revealed that the brown epibionts of “P. roseum” constituted up to 37% of the total bacterial cell number and up to 88% of all green sulfur bacteria present in the chemocline. Specific amplification of 16S rRNA gene fragments of green sulfur bacteria and denaturing gradient gel electrophoresis fingerprinting yielded a maximum of four different DNA bands depending on the year of study, indicating that the diversity of green sulfur bacteria was low. The 465-bp 16S rRNA gene sequence of the epibiont of “P. roseum” was obtained after sorting of individual consortia by micromanipulation, followed by a highly sensitive PCR. The sequence obtained represents a new phylotype within the radiation of green sulfur bacteria. Maximum light-dependent H14CO3 − fixation in the chemocline in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea suggested that there was anaerobic autotrophic growth of the green sulfur bacteria. The metabolism of the epibionts was further studied by determining stable carbon isotope ratios (δ13C) of their specific biomarkers. Analysis of photosynthetic pigments by high-performance liquid chromatography revealed the presence of high concentrations of bacteriochlorophyll (BChl) e and smaller amounts of BChl a and d and chlorophyll a in the chemocline. Unexpectedly, isorenieratene and β-isorenieratene, carotenoids typical of other brown members of the green sulfur bacteria, were absent. Instead, four different esterifying alcohols of BChl e were isolated as biomarkers of green sulfur bacterial epibionts, and their δ13C values were determined. Farnesol, tetradecanol, hexadecanol, and hexadecenol all were significantly enriched in 13C compared to bulk dissolved and particulate organic carbon and compared to the biomarkers of purple sulfur bacteria. The difference between the δ13C values of farnesol, the major esterifying alcohol of BChl e, and CO2 was −7.1%, which provides clear evidence that the mode of growth of the green sulfur bacterial epibionts of “P. roseum” in situ is photoautotrophic.


2010 ◽  
Vol 60 (6) ◽  
pp. 1376-1382 ◽  
Author(s):  
Takao Iino ◽  
Koji Mori ◽  
Yoshihito Uchino ◽  
Tatsunori Nakagawa ◽  
Shigeaki Harayama ◽  
...  

A moderately thermophilic chemoheterotrophic bacterium, strain Mat9-16T, was isolated from microbial mats developed in hot spring water streams from Yumata, Nagano, Japan. Cells of strain Mat9-16T were strictly anaerobic, Gram-stain-negative, non-sporulating, non-motile and short to long rods (2.0–15.5 μm in length). Strain Mat9-16T grew fermentatively with optimum growth at 45 °C, pH 7.0–7.5 and 1 % NaCl (w/v). Phylogenetic analysis based on the 16S rRNA gene revealed that strain Mat9-16T was affiliated with an uncultivated lineage, and the nearest cultivated neighbours were green sulfur bacteria belonging to the class Chlorobea with 77–83 % sequence similarity. However, strain Mat9-16T could not grow phototrophically and did not possess light-harvesting structures, morphologically and genetically, such as the chlorosomes of green sulfur bacteria. On the basis of phenotypic features and phylogenetic position, a novel genus and species are proposed for strain Mat9-16T, to be named Ignavibacterium album gen. nov., sp. nov. (=NBRC 101810T =DSM 19864T). We also propose to place the cultivated bacterial lineage accommodating the sole representative Mat9-16T in a novel class, Ignavibacteria classis nov. In addition, we present a formal description of the phylum-level taxon ‘Chlorobi’ as Chlorobi phyl. nov.


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