MicRhoDE: a curated database for the analysis of microbial rhodopsin diversity and evolution

Bœuf, Dominique Le; Audic, Stéphane; Brillet-Guéguen, Loraine; Caron, Christophe; Jeanthon, Christian

doi:10.1093/database/bav080

Cited by 48 publications

(59 citation statements)

References 46 publications

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“…Moreover, since amino acid sequences have diverged considerably, alignments for phylogenetic analyses are delicate, and inferred trees are sensitive to which sequences are included. There is as yet no comprehensive phylogenetic tree of rhodopsins in the literature, although a database (MicRhoDE) for phylogenetic analysis of microbial rhodopsins was presented in June 2015 (39). Figure 2 shows our best effort to build a robust tree with all the different types of type I rhodopsins known in March 2016.…”

Section: Rhodopsin Typesmentioning

confidence: 99%

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

171

172

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SUMMARYThe recognition of a new family of rhodopsins in marine planktonic bacteria, proton-pumping proteorhodopsin, expanded the known phylogenetic range, environmental distribution, and sequence diversity of retinylidene photoproteins. At the time of this discovery, microbial ion-pumping rhodopsins were known solely in haloarchaea inhabiting extreme hypersaline environments. Shortly thereafter, proteorhodopsins and other light-activated energy-generating rhodopsins were recognized to be widespread among marine bacteria. The ubiquity of marine rhodopsin photosystems now challenges prior understanding of the nature and contributions of “heterotrophic” bacteria to biogeochemical carbon cycling and energy fluxes. Subsequent investigations have focused on the biophysics and biochemistry of these novel microbial rhodopsins, their distribution across the tree of life, evolutionary trajectories, and functional expression in nature. Later discoveries included the identification of proteorhodopsin genes in all three domains of life, the spectral tuning of rhodopsin variants to wavelengths prevailing in the sea, variable light-activated ion-pumping specificities among bacterial rhodopsin variants, and the widespread lateral gene transfer of biosynthetic genes for bacterial rhodopsins and their associated photopigments. Heterologous expression experiments with marine rhodopsin genes (and associated retinal chromophore genes) provided early evidence that light energy harvested by rhodopsins could be harnessed to provide biochemical energy. Importantly, some studies with native marine bacteria show that rhodopsin-containing bacteria use light to enhance growth or promote survival during starvation. We infer from the distribution of rhodopsin genes in diverse genomic contexts that different marine bacteria probably use rhodopsins to support light-dependent fitness strategies somewhere between these two extremes.

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Section: Rhodopsin Typesmentioning

confidence: 99%

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

171

172

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“…Another study separated five different subclades of MGII proteorhodopsin (Tully, 2019) following nomenclature from (Boeuf, Audic, Brillet-Guéguen, Caron, & Jeanthon, 2015;Pinhassi, DeLong, Béjà, González, & Pedrós-Alió, 2016). Other metagenomics fragments suggest that some MGIIa could live associated to particles, and that they could be motile and degrade polymers like proteins and lipids (Iverson et al, 2012;Rinke et al, 2018;Tully, 2019;Xie et al, 2018).…”

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confidence: 99%

Genomic ecology of Marine Group II, the most common marine planktonic Archaea across the surface ocean

et al. 2019

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Planktonic Archaea have been detected in all the world's oceans and are found from surface waters to the deep sea. The two most common Archaea phyla are Thaumarchaeota and Euryarchaeota. Euryarchaeota are generally more common in surface waters, but very little is known about their ecology and their potential metabolisms. In this study, we explore the genomic ecology of the Marine Group II (MGII), the main marine planktonic Euryarchaeota, and test if it is composed of different ecologically relevant units. We re‐analyzed Tara Oceans metagenomes from the photic layer and the deep ocean by annotating sequences against a custom MGII database and by mapping gene co‐occurrences. Our data provide a global view of the distribution of Euryarchaeota, and more specifically of MGII subgroups, and reveal their association to a number of gene‐coding sequences. In particular, we show that MGII proteorhodopsins were detected in both the surface and the deep chlorophyll maximum layer and that different clusters of these light harvesting proteins were present. Our approach helped describing the set of genes found together with specific MGII subgroups. We could thus define genomic environments that could theoretically describe ecologically meaningful units and the ecological niche that they occupy.

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“…Predicted proteins of each genome were screened for matches to the rhodopsin PFAM model (PF01036; hmmsearch -T 75; Supplemental Data 8). In order to identify putative proteorhodopsins, sequences matching the 415 rhodopsin HMM model were processed using the Galaxy-MICrhoDE workflow implemented on the Galaxy web server (http://usegalaxy.org) to assign rhodopsins to the MICrhoDE database 53 . The alignment generated from the workflow was manually trimmed to a 96 amino acid region conserved across all sequences, re-aligned using MUSCLE and used to construct a phylogenetic tree with FastTree (as above; Supplemental Data 9).…”

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confidence: 99%

Metabolic Diversity within the Globally Abundant Marine Group IIEuryarchaeaOffers Insight into Ecological Patterns

Tully

2018

Preprint

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Despite their discovery over 25 years ago, the Marine Group II Euryarchaea (MGII) have remained a difficult group of organisms to study, lacking cultured isolates and genome references. The MGII have 10 been identified in marine samples from around the world and evidence supports a photoheterotrophic lifestyle combining phototrophy via proteorhodopsins with the remineralization of high molecular weight organic matter. Divided between two Orders, the MGII have distinct ecological patterns that are not understood based on the limited number of available genomes. Here, we present the comparative genomic analysis of 322 MGII genomes, providing the most detailed view of these mesophilic archaea to-date. 15This analysis identified 17 distinct Family level clades including nine clades that previously lacked reference genomes. The metabolic potential and ecological distribution of the MGII genera revealed distinct roles in the environment, identifying algal-saccharide-degrading coastal genera, protein-degrading oligotrophic surface ocean genera, and mesopelagic genera lacking proteorhodopsins common in all other families. This study redefines the MGII and provides an avenue for understanding the role these 20 organisms play in the cycling of organic matter throughout the water column. Main textSince their discovery by DeLong 1 (1992), despite global distribution and representing a significant portion of the microbial plankton in the photic zone, the Marine Group II (MGII) Euryarchaea 25have remained an enigmatic group of organisms in the marine the environment. The MGII have been predominantly identified in the surface oceans 2 , account for ~15% of the archaeal cells in the oligotrophic open ocean 3 , and shown to increase in abundance in response to phytoplankton blooms 4 comprising up to ~30% of the total microbial community 5 . Research has shown that the MGII correspond with specific genera of phytoplankton 6 , during and after blooms 7 , and can be associated with particles when samples 30 are size fractionated 8 . Phylogenetic analyses have revealed the presence of two dominant clades of MGII, referred to as MGIIA and MGIIB (the MGIIB have recently been named Thalassoarchaea 9 ), that respond to different environmental conditions, including temperature and nutrients 10 . To date, the MGII have not been successfully cultured or enriched from the marine environment. Instead our current understanding of the role these organisms play in the environment is derived from 35interpretations of ecological data (i.e., phytoplankton-and particle-associated) and a limited number of genomic fragments and reconstructed environmental genomes. Collectively, these genomic studies have revealed a number of re-occurring traits common to the MGII, including: proteorhodopsins in MGII sampled from the photic zone 11 , genes targeting the degradation of high molecular weight (HMW) organic matter, such as proteins, carbohydrates, and lipids, and subsequent transport of constituent 40 components into the cell 9,12-14 , genes representative...

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MicRhoDE: a curated database for the analysis of microbial rhodopsin diversity and evolution

Cited by 48 publications

References 46 publications

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Genomic ecology of Marine Group II, the most common marine planktonic Archaea across the surface ocean

Metabolic Diversity within the Globally Abundant Marine Group IIEuryarchaeaOffers Insight into Ecological Patterns

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