Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota.
ABSTRACT: Horizontal gene transfer (HGT) is an important force in evolution, which may lead, among other things, to the adaptation to new environments by the import of new metabolic functions. Recent studies based on phylogenetic analyses of a few genome fragments containing archaeal 16S rRNA genes and fosmid-end sequences from deep-sea metagenomic libraries have suggested that marine planktonic archaea could be affected by high HGT frequency. Likewise, a composite genome of an uncultured marine euryarchaeote showed high levels of gene sequence similarity to bacterial genes. In this work, we ask whether HGT is frequent and widespread in genomes of these marine archaea, and whether HGT is an ancient and/or recurrent phenomenon. To answer these questions, we sequenced 997 fosmid archaeal clones from metagenomic libraries of deep-Mediterranean waters (1,000 and 3,000 m depth) and built comprehensive pangenomes for planktonic Thaumarchaeota (Group I archaea) and Euryarchaeota belonging to the uncultured Groups II and III Euryarchaeota (GII/III-Euryarchaeota). Comparison with available reference genomes of Thaumarchaeota and a composite marine surface euryarchaeote genome allowed us to define sets of core, lineage-specific core, and shell gene ortholog clusters for the two archaeal lineages. Molecular phylogenetic analyses of all gene clusters showed that 23.9% of marine Thaumarchaeota genes and 29.7% of GII/III-Euryarchaeota genes had been horizontally acquired from bacteria. HGT is not only extensive and directional but also ongoing, with high HGT levels in lineage-specific core (ancient transfers) and shell (recent transfers) genes. Many of the acquired genes are related to metabolism and membrane biogenesis, suggesting an adaptive value for life in cold, oligotrophic oceans. We hypothesize that the acquisition of an important amount of foreign genes by the ancestors of these archaeal groups significantly contributed to their divergence and ecological success.
Project description:The extent of horizontal gene transfer (HGT) among marine pelagic prokaryotes and the role that HGT may have played in their adaptation to this particular environment remain open questions. This is partly due to the paucity of cultured species and genomic information for many widespread groups of marine bacteria and archaea. Molecular studies have revealed a large diversity and relative abundance of marine planktonic archaea, in particular of Thaumarchaeota (also known as group I Crenarchaeota) and Euryarchaeota of groups II and III, but only one species (the thaumarchaeote Candidatus Nitrosopumilus maritimus) has been isolated in pure culture so far. Therefore, metagenomics remains the most powerful approach to study these environmental groups. To investigate the impact of HGT in marine archaea, we carried out detailed phylogenetic analyses of all open reading frames of 21 archaeal 16S rRNA gene-containing fosmids and, to extend our analysis to other genomic regions, also of fosmid-end sequences of 12?774 fosmids from three different deep-sea locations (South Atlantic and Adriatic Sea at 1000?m depth, and Ionian Sea at 3000?m depth). We found high HGT rates in both marine planktonic Thaumarchaeota and Euryarchaeota, with remarkable converging values estimated from complete-fosmid and fosmid-end sequence analysis (25 and 21% of the genes, respectively). Most HGTs came from bacterial donors (mainly from Proteobacteria, Firmicutes and Chloroflexi) but also from other archaea and eukaryotes. Phylogenetic analyses showed that in most cases HGTs are shared by several representatives of the studied groups, implying that they are ancient and have been conserved over relatively long evolutionary periods. This, together with the functions carried out by these acquired genes (mostly related to energy metabolism and transport of metabolites across membranes), suggests that HGT has played an important role in the adaptation of these archaea to the cold and nutrient-depleted deep marine environment.
Project description:The Archaea domain is ubiquitously distributed and extremely diverse, however, environmental factors that shape archaeal community structure are not well known. Aquatic environments, including the water column and sediments harbor many new uncultured archaeal species from which metabolic and ecological roles remain elusive. Some environments are especially neglected in terms of archaeal diversity, as is the case of pristine tropical areas. Here we investigate the archaeal composition in marine and freshwater systems from Ilha Grande, a South Atlantic tropical environment. All sampled habitats showed high archaeal diversity. No OTUs were shared between freshwater, marine and mangrove sediment samples, yet these environments are interconnected and geographically close, indicating environment-specific community structuring. Group II Euryarchaeota was the main clade in marine samples, while the new putative phylum Thaumarchaeota and LDS/RCV Euryarchaeota dominated freshwaters. Group III Euryarchaeota, a rare clade, was also retrieved in reasonable abundance in marine samples. The archaeal community from mangrove sediments was composed mainly by members of mesophilic Crenarchaeota and by a distinct clade forming a sister-group to Crenarchaeota and Thaumarchaeota. Our results show strong environment-specific community structuring in tropical aquatic Archaea, as previously seen for Bacteria.
Project description:It is widely believed that the archaeal ancestor was hyperthermophilic, but during archaeal evolution, several lineages - including haloarchaea and their sister methanogens, the Thaumarchaeota, and the uncultured Marine Group II and Marine Group III Euryarchaeota (MGII/III) - independently adapted to lower temperatures. Recent phylogenomic studies suggest that the ancestors of these lineages were recipients of massive horizontal gene transfer from bacteria. Many of the acquired genes, which are often involved in metabolism and cell envelope biogenesis, were convergently acquired by distant mesophilic archaea. In this Opinion article, we explore the intriguing hypothesis that the import of these bacterial genes was crucial for the adaptation of archaea to mesophilic lifestyles.
Project description:Archaea are ubiquitous in marine plankton, and fossil forms of archaeal tetraether membrane lipids in sedimentary rocks document their participation in marine biogeochemical cycles for >100 million years. Ribosomal RNA surveys have identified four major clades of planktonic archaea but, to date, tetraether lipids have been characterized in only one, the Marine Group I Thaumarchaeota. The membrane lipid composition of the other planktonic archaeal groups--all uncultured Euryarchaeota--is currently unknown. Using integrated nucleic acid and lipid analyses, we found that Marine Group II Euryarchaeota (MG-II) contributed significantly to the tetraether lipid pool in the North Pacific Subtropical Gyre at shallow to intermediate depths. Our data strongly suggested that MG-II also synthesize crenarchaeol, a tetraether lipid previously considered to be a unique biomarker for Thaumarchaeota. Metagenomic datasets spanning 5 y indicated that depth stratification of planktonic archaeal groups was a stable feature in the North Pacific Subtropical Gyre. The consistent prevalence of MG-II at depths where the bulk of exported organic matter originates, together with their ubiquitous distribution over diverse oceanic provinces, suggests that this clade is a significant source of tetraether lipids to marine sediments. Our results are relevant to archaeal lipid biomarker applications in the modern oceans and the interpretation of these compounds in the geologic record.
Project description:The Archaea are a widely distributed group of prokaryotes that inhabit and thrive in many different environments. In the sea, they play key roles in various global biogeochemical processes. Here, in order to investigate the vertical profiles of archaeal community across a large geographic distance, the compositions of archaeal communities in seven seawater columns in the Pacific Ocean were investigated using high throughput 454 pyrosequencing of the 16S rRNA gene. The surface archaeal communities showed lower diversity and greater variability than those in the deeper layers. Two of the major archaeal phyla that displayed different depth preferences were Thaumarchaeota and Euryarchaeota. The majority of Thaumarchaeota belonged to Marine Group I (MGI), which had high relative abundance in deep water. In contrast, Euryarchaeota, which mainly consisted of Marine Group II (MGII) and III (MGIII), were dominant in the surface layer. Compared with MGI and MGII, MGIII were less abundant in seawater and generally absent from the surface water of the subarctic Pacific. In addition, niche separation in the MGI, MGII, and MGIII subgroups was also observed. For example, MGI.C and MGII.A (the major subgroups of MGI and MGII, respectively) displayed a strong negative correlation with each other. The highest level of archaeal diversity was found in the core of an oxygen minimum zone (OMZ) located off Costa Rica, which resulted from the co-occurrence of both anaerobic and aerobic archaea. For example, methanotrophic archaea ANME-2, methanogenic archaea and several sediment origin archaea, such as Marine Benthic Group A (MBGA) and Bathyarchaeota, were all detected at relatively high abundance in the OMZ. Together, our findings indicate that vertical heterogeneities along water columns and latitudinal differentiation in the surface waters are ubiquitous features of archaeal communities in the Pacific Ocean, and the OMZ off Costa Rica is an archaeal biodiversity hot-spot.
Project description:Archaea are widespread in marine sediments, but their occurrence and relationship with natural salinity gradients in estuarine sediments is not well understood. This study investigated the abundance and diversity of Archaea in sediments at three sites [Brightlingsea (BR), Alresford (AR) and Hythe (HY)] along the Colne Estuary, using quantitative real-time PCR (qPCR) of 16S rRNA genes, DNA hybridization, Archaea 16S rRNA and mcrA gene phylogenetic analyses. Total archaeal 16S rRNA abundance in sediments were higher in the low-salinity brackish sediments from HY (2-8 × 10(7) 16S rRNA gene copies cm(-3)) than the high-salinity marine sites from BR and AR (2 × 10(4)-2 × 10(7) and 4 × 10(6)-2 × 10(7) 16S rRNA gene copies cm(-3), respectively), although as a proportion of the total prokaryotes Archaea were higher at BR than at AR or HY. Phylogenetic analysis showed that members of the 'Bathyarchaeota' (MCG), Thaumarchaeota and methanogenic Euryarchaeota were the dominant groups of Archaea. The composition of Thaumarchaeota varied with salinity, as only 'marine' group I.1a was present in marine sediments (BR). Methanogen 16S rRNA genes from low-salinity sediments at HY were dominated by acetotrophic Methanosaeta and putatively hydrogentrophic Methanomicrobiales, whereas the marine site (BR) was dominated by mcrA genes belonging to methylotrophic Methanococcoides, versatile Methanosarcina and methanotrophic ANME-2a. Overall, the results indicate that salinity and associated factors play a role in controlling diversity and distribution of Archaea in estuarine sediments.
Project description:The marine pelagic archaeal community is dominated by three major groups, the marine group I (MGI) Thaumarchaeota, and the marine groups II and III (MGII and MGIII) Euryarchaeota. Studies of both MGI cultures and the environment have shown that the MGI core membrane lipids are predominantly composed of glycerol dibiphytanyl glycerol tetraether (GDGT) lipids and the diether lipid archaeol. However, there are no cultured representatives of MGII and III archaea and, therefore, both their membrane lipid composition and potential contribution to the marine archaeal lipid pool remain unknown. Here, we show that GDGTs present in suspended particulate matter of the (sub)surface waters of the North Atlantic Ocean and the coastal North Sea are derived from MGI archaea, and that MGII archaea do not significantly contribute to the pool of GDGTs and archaeol. This implies, in contrast to previous suggestions, that their lipids do not affect the widely used sea surface temperature proxy TEX<sub>86</sub>. These findings also indicate that MGII archaea are not able to produce any known archaeal lipids, implying that our understanding of the evolution of membrane lipid biosynthesis in Archaea is far from complete.
Project description:Archaea play an important role in various biogeochemical cycles. They are known extremophiles inhabiting environments such as thermal springs or hydrothermal vents. Recent studies have revealed a significant abundance of Archaea in moderate environments, for example, temperate sea water. Nevertheless, the composition and ecosystem function of these marine archaeal communities is largely unknown. To assess diversity and composition of active archaeal communities in the German Bight, seven marine water samples were taken and studied by RNA-based analysis of ribosomal 16S rRNA. For this purpose, total RNA was extracted from the samples and converted to cDNA. Archaeal community structures were investigated by pyrosequencing-based analysis of 16S rRNA amplicons generated from cDNA. To our knowledge, this is the first study combining next-generation sequencing and metatranscriptomics to study archaeal communities in marine habitats. The pyrosequencing-derived dataset comprised 62,045 archaeal 16S rRNA sequences. We identified Halobacteria as the predominant archaeal group across all samples with increased abundance in algal blooms. Thermoplasmatales (Euryarchaeota) and the Marine Group I (Thaumarchaeota) were identified in minor abundances. It is indicated that archaeal community patterns were influenced by environmental conditions.
Project description:Archaea are important players in marine biogeochemical cycles, and their membrane lipids are useful biomarkers in environmental and geobiological studies. However, many archaeal groups remain uncultured and their lipid composition unknown. Here, we aim to expand the knowledge on archaeal lipid biomarkers and determine the potential sources of those lipids in the water column of the euxinic Black Sea. The archaeal community was evaluated by 16S rRNA gene amplicon sequencing and by quantitative PCR. The archaeal intact polar lipids (IPLs) were investigated by ultra-high-pressure liquid chromatography coupled to high-resolution mass spectrometry. Our study revealed both a complex archaeal community and large changes with water depth in the IPL assemblages. In the oxic/upper suboxic waters (<105 m), the archaeal community was dominated by marine group (MG) I Thaumarchaeota, coinciding with a higher relative abundance of hexose phosphohexose crenarchaeol, a known marker for Thaumarchaeota. In the suboxic waters (80-110 m), MGI Nitrosopumilus sp. dominated and produced predominantly monohexose glycerol dibiphytanyl glycerol tetraethers (GDGTs) and hydroxy-GDGTs. Two clades of MGII Euryarchaeota were present in the oxic and upper suboxic zones in much lower abundances, preventing the detection of their specific IPLs. In the deep sulfidic waters (>110 m), archaea belonging to the DPANN Woesearchaeota, Bathyarchaeota, and ANME-1b clades dominated. Correlation analyses suggest that the IPLs GDGT-0, GDGT-1, and GDGT-2 with two phosphatidylglycerol (PG) head groups and archaeol with a PG, phosphatidylethanolamine, and phosphatidylserine head groups were produced by ANME-1b archaea. Bathyarchaeota represented 55% of the archaea in the deeper part of the euxinic zone and likely produces archaeol with phospho-dihexose and hexose-glucuronic acid head groups.
Project description:Marine Archaea are important players among microbial plankton and significantly contribute to biogeochemical cycles, but details regarding their community structure and long-term seasonal activity and dynamics remain largely unexplored. In this study, we monitored the interannual archaeal community composition of abundant and rare biospheres in northwestern Mediterranean Sea surface waters by pyrosequencing 16S rDNA and rRNA. A detailed analysis of the rare biosphere structure showed that the rare archaeal community was composed of three distinct fractions. One contained the rare Archaea that became abundant at different times within the same ecosystem; these cells were typically not dormant, and we hypothesize that they represent a local seed bank that is specific and essential for ecosystem functioning through cycling seasonal environmental conditions. The second fraction contained cells that were uncommon in public databases and not active, consisting of aliens to the studied ecosystem and representing a nonlocal seed bank of potential colonizers. The third fraction contained Archaea that were always rare but actively growing; their affiliation and seasonal dynamics were similar to the abundant microbes and could not be considered a seed bank. We also showed that the major archaeal groups, Thaumarchaeota marine group I and Euryarchaeota group II.B in winter and Euryarchaeota group II.A in summer, contained different ecotypes with varying activities. Our findings suggest that archaeal diversity could be associated with distinct metabolisms or life strategies, and that the rare archaeal biosphere is composed of a complex assortment of organisms with distinct histories that affect their potential for growth.