An official website of the United States government
Abstract Rhodopsin photosystems convert light energy into electrochemical gradients used by the cell to produce ATP, or for other energy-demanding processes. While these photosystems are widespread in the ocean and have been identified in diverse microbial taxonomic groups, their physiological role in vivo has only been studied in few marine bacterial strains. Recent metagenomic studies revealed the presence of rhodopsin genes in the understudied Verrucomicrobiota phylum, yet their distribution within different Verrucomicrobiota lineages, their diversity, and function remain unknown. In this study, we show that more than 7% of Verrucomicrobiota genomes (n = 2916) harbor rhodopsins of different types. Furthermore, we describe the first two cultivated rhodopsin-containing strains, one harboring a proteorhodopsin gene and the other a xanthorhodopsin gene, allowing us to characterize their physiology under laboratory-controlled conditions. The strains were isolated in a previous study from the Eastern Mediterranean Sea and read mapping of 16S rRNA gene amplicons showed the highest abundances of these strains at the deep chlorophyll maximum (source of their inoculum) in winter and spring, with a substantial decrease in summer. Genomic analysis of the isolates suggests that motility and degradation of organic material, both energy demanding functions, may be supported by rhodopsin phototrophy in Verrucomicrobiota. Under culture conditions, we show that rhodopsin phototrophy occurs under carbon starvation, with light-mediated energy generation supporting sugar transport into the cells. Overall, this study suggests that photoheterotrophic Verrucomicrobiota may occupy an ecological niche where energy harvested from light enables bacterial motility toward organic matter and supports nutrient uptake.
more »
« less
Diversity, distribution, and expression of opsin genes in freshwater lakes
Abstract Microbial rhodopsins are widely distributed in aquatic environments and may significantly contribute to phototrophy and energy budgets in global oceans. However, the study of freshwater rhodopsins has been largely limited. Here, we explored the diversity, ecological distribution, and expression of opsin genes that encode the apoproteins of type I rhodopsins in humic and clearwater lakes with contrasting physicochemical and optical characteristics. Using metagenomes and metagenome‐assembled genomes, we recovered opsin genes from a wide range of taxa, mostly predicted to encode green light‐absorbing proton pumps. Viral opsin and novel bacterial opsin clades were recovered. Opsin genes occurred more frequently in taxa from clearwater than from humic water, and opsins in some taxa have nontypical ion‐pumping motifs that might be associated with physicochemical conditions of these two freshwater types. Analyses of the surface layer of 33 freshwater systems revealed an inverse correlation between opsin gene abundance and lake dissolved organic carbon (DOC). In humic water with high terrestrial DOC and light‐absorbing humic substances, opsin gene abundance was low and dramatically declined within the first few meters, whereas the abundance remained relatively high along the bulk water column in clearwater lakes with low DOC, suggesting opsin gene distribution is influenced by lake optical properties and DOC. Gene expression analysis confirmed the significance of rhodopsin‐based phototrophy in clearwater lakes and revealed different diel expressional patterns among major phyla. Overall, our analyses revealed freshwater opsin diversity, distribution and expression patterns, and suggested the significance of rhodopsin‐based phototrophy in freshwater energy budgets, especially in clearwater lakes.
more »
« less
- PAR ID:
- 10415071
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 32
- Issue:
- 11
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 2798-2817
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)Abstract Microbial sulfur metabolism contributes to biogeochemical cycling on global scales. Sulfur metabolizing microbes are infected by phages that can encode auxiliary metabolic genes (AMGs) to alter sulfur metabolism within host cells but remain poorly characterized. Here we identified 191 phages derived from twelve environments that encoded 227 AMGs for oxidation of sulfur and thiosulfate ( dsrA , dsrC/tusE , soxC , soxD and soxYZ ). Evidence for retention of AMGs during niche-differentiation of diverse phage populations provided evidence that auxiliary metabolism imparts measurable fitness benefits to phages with ramifications for ecosystem biogeochemistry. Gene abundance and expression profiles of AMGs suggested significant contributions by phages to sulfur and thiosulfate oxidation in freshwater lakes and oceans, and a sensitive response to changing sulfur concentrations in hydrothermal environments. Overall, our study provides fundamental insights on the distribution, diversity, and ecology of phage auxiliary metabolism associated with sulfur and reinforces the necessity of incorporating viral contributions into biogeochemical configurations.more » « less
-
null (Ed.)Abstract. Outgassing of carbon dioxide (CO2) from freshwater ecosystems comprises 12 %–25 % of the total carbon flux from soils and bedrock. This CO2 is largely derived from both biodegradation and photodegradation of terrestrial dissolved organic carbon (DOC) entering lakes from wetlands and soils in the watersheds of lakes. In spite of the significance of these two processes in regulating rates of CO2 outgassing, their relative importance remains poorly understood in lake ecosystems. In this study, we used groundwater from the watersheds of one subtropical and three temperate lakes of differing trophic status to simulate the effects of increases in terrestrial DOC from storm events. We assessed the relative importance of biodegradation and photodegradation in oxidizing DOC to CO2. We measured changes in DOC concentration, colored dissolved organic carbon (specificultraviolet absorbance – SUVA320; spectral slope ratio – Sr), dissolved oxygen, and dissolved inorganic carbon (DIC) in short-term experiments from May–August 2016. In all lakes, photodegradationled to larger changes in DOC and DIC concentrations and opticalcharacteristics than biodegradation. A descriptive discriminant analysisshowed that, in brown-water lakes, photodegradation led to the largestdeclines in DOC concentration. In these brown-water systems, ∼ 30 % of the DOC was processed by sunlight, and a minimum of 1 % was photomineralized. In addition to documenting the importance of photodegradation in lakes, these results also highlight how lakes in the future may respond to changes in DOC inputs.more » « less
-
The rapid climate warming is affecting the Arctic which is rich in aquatic systems. As a result of permafrost thaw, thermokarst lakes and ponds are either shrinking due to lake drainage or expanding due to lake shore erosion. This process in turn mobilizes organic carbon, which is released by permafrost deposits and active layer material that slips into the lake. In this study, we combine hydrochemical measurements and remote sensing data to analyze the influence of lake change processes, especially lake growth, on lake hydrochemical parameters such as DOC, EC, pH as well as stable oxygen and hydrogen isotopes in the Arctic Coastal Plain. For our entire dataset of 97 water samples from 82 water bodies, we found significantly higher CH4 concentrations in lakes with a floating-ice regime and significantly higher DOC concentrations in lakes with a bedfast-ice regime. We show significantly lower CH4 concentrations in lagoons compared to lakes as a result of an effective CH4 oxidation that increased with a seawater connection. For our detailed lake sampling of two thermokarst lakes, we found a significant positive correlation for lake shore erosion and DOC for one of the lakes. Our detailed lake sampling approach indicates that the generally shallow thermokarst lakes are overall well mixed and that single hydrochemical samples are representative for the entire lake. Finally, our study confirms that DOC concentrations correlates with lake size, ecoregion type and underlying deposits.more » « less
-
Many marine organisms have a biphasic life cycle that transitions between a swimming larva with a more sedentary adult form. At the end of the first phase, larvae must identify suitable sites to settle and undergo a dramatic morphological change. Environmental factors, including photic and chemical cues, appear to influence settlement, but the sensory receptors involved are largely unknown. We targeted the protein receptor, opsin, which belongs to large superfamily of transmembrane receptors that detects environmental stimuli, hormones, and neurotransmitters. While opsins are well-known for light-sensing, including vision, a growing number of studies have demonstrated light-independent functions. We therefore examined opsin expression in the Pteriomorphia, a large, diverse clade of marine bivalves, that includes commercially important species, such as oysters, mussels, and scallops. Methods Genomic annotations combined with phylogenetic analysis show great variation of opsin abundance among pteriomorphian bivalves, including surprisingly high genomic abundance in many species that are eyeless as adults, such as mussels. Therefore, we investigated the diversity of opsin expression from the perspective of larval development. We collected opsin gene expression in four families of Pteriomorphia, across three distinct larval stages, i.e., trochophore, veliger, and pediveliger, and compared those to adult tissues.Results We found larvae express all opsin types in these bivalves, but opsin expression patterns are largely species-specific across development. Few opsins are expressed in the adult mantle, but many are highly expressed in adult eyes. Intriguingly, opsin genes such as retinochrome, xenopsins, and Go-opsins have higher levels of expression in the later larval stages when substrates for settlement are being tested, such as the pediveliger. Conclusion Investigating opsin gene expression during larval development provides crucial insights into their intricate interactions with the surroundings, which may shed light on how opsin receptors of these organisms respond to various environmental cues that play a pivotal role in their settlement process.more » « less
