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Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns.

ABSTRACT: Despite their discovery over 25 years ago, the Marine Group II Euryarchaea (MGII) remain a difficult group of organisms to study, lacking cultured isolates and genome references. The MGII have 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 clades, the MGII have distinct ecological patterns that are not understood based on the limited number of available genomes. Here, I present a comparative genomic analysis of 250 MGII genomes, providing a comprehensive investigation of these mesophilic archaea. This analysis identifies 17 distinct subclades including nine subclades that previously lacked reference genomes. The metabolic potential and distribution of the MGII genera reveals distinct roles in the environment, identifying algal-saccharide-degrading coastal subclades, protein-degrading oligotrophic surface ocean subclades, and mesopelagic subclades lacking proteorhodopsins, common in all other subclades.

SUBMITTER: Tully BJ

PROVIDER: S-EPMC6336850 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns.

Tully Benjamin J BJ

Nature communications 20190117 1

Despite their discovery over 25 years ago, the Marine Group II Euryarchaea (MGII) remain a difficult group of organisms to study, lacking cultured isolates and genome references. The MGII have 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 clades, the MGII have distinct ecological patterns that are not und ...[more]

PMID: 30655514

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Project description:Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

Project description:The impact of predator-prey interactions on the evolution of many marine invertebrates is poorly understood. Since barriers to genetic exchange are less obvious in the marine realm than in terrestrial or freshwater systems, non-allopatric divergence may play a fundamental role in the generation of biodiversity. In this context, shifts between major prey types could constitute important factors explaining the biodiversity of marine taxa, particularly in groups with highly specialized diets. However, the scarcity of marine specialized consumers for which reliable phylogenies exist hampers attempts to test the role of trophic specialization in evolution. In this study, RNA-Seq data is used to produce a phylogeny of Cladobranchia, a group of marine invertebrates that feed on a diverse array of prey taxa but mostly specialize on cnidarians. The broad range of prey type preferences allegedly present in two major groups within Cladobranchia suggest that prey type shifts are relatively common over evolutionary timescales.In the present study, we generated a well-supported phylogeny of the major lineages within Cladobranchia using RNA-Seq data, and used ancestral state reconstruction analyses to better understand the evolution of prey preference. These analyses answered several fundamental questions regarding the evolutionary relationships within Cladobranchia, including support for a clade of species from Arminidae as sister to Tritoniidae (which both preferentially prey on Octocorallia). Ancestral state reconstruction analyses supported a cladobranchian ancestor with a preference for Hydrozoa and show that the few transitions identified only occur from lineages that prey on Hydrozoa to those that feed on other types of prey.There is strong phylogenetic correlation with prey preference within Cladobranchia, suggesting that prey type specialization within this group has inertia. Shifts between different types of prey have occurred rarely throughout the evolution of Cladobranchia, indicating that this may not have been an important driver of the diversity within this group.

Project description:Particles in aquatic environments host distinct communities of microbes, yet the evolution of particle-specialized taxa and the extent to which specialized microbial metabolism is associated with particles is largely unexplored. Here, we investigate the hypothesis that a widely distributed and uncultivated microbial group--the marine group II euryarchaea (MGII)--interacts with living and detrital particulate organic matter (POM) in the euphotic zone of the central California Current System. Using fluorescent in situ hybridization, we verified the association of euryarchaea with POM. We further quantified the abundance and distribution of MGII 16?S ribosomal RNA genes in size-fractionated seawater samples and compared MGII functional capacity in metagenomes from the same fractions. The abundance of MGII in free-living and >3??m fractions decreased with increasing distance from the coast, whereas MGII abundance in the 0.8-3??m fraction remained constant. At several offshore sites, MGII abundance was highest in particle fractions, indicating that particle-attached MGII can outnumber free-living MGII under oligotrophic conditions. Compared with free-living MGII, the genome content of MGII in particle-associated fractions exhibits an increased capacity for surface adhesion, transcriptional regulation and catabolism of high molecular weight substrates. Moreover, MGII populations in POM fractions are phylogenetically distinct from and more diverse than free-living MGII. Eukaryotic phytoplankton additions stimulated MGII growth in bottle incubations, providing the first MGII net growth rate measurements. These ranged from 0.47 to 0.54?d(-1). However, MGII were not recovered in whole-genome amplifications of flow-sorted picoeukaryotic phytoplankton and heterotrophic nanoflagellates, suggesting that MGII in particle fractions are not physically attached to living POM. Collectively, our results support a linkage between MGII ecophysiology and POM, implying that marine archaea have a role in elemental cycling through interactions with particles.

Dataset Information

Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns.

Publications

Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns.

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