Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column
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Keywords:
Thaumarchaeota
Ecotype
Thaumarchaeota
Epilimnion
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Abstract Nitrification plays a key role in marine ecosystems where Thaumarchaeota are thought to be responsible for most of the ammonia oxidation in the water column. Over a 2‐yr, near‐monthly time series at two sites in Monterey Bay we observed repeatable seasonal and depth‐based patterns of Thaumarchaeota ecotype abundance that highlighted a clear delineation between populations in shallow euphotic (< 50 m) vs. deeper mesopelagic (60–500 m) depths. Euphotic depths show greater seasonality and influence from light, while mesopelagic waters have trends based on water mass and other covarying features with depth. Three major ecotypes were recovered: a Nitrosopumilus ‐like (NP) group, a Nitrosopelagicus ‐like ecotype containing “shallow” water column A (WCA) members, and an ecotype affiliated with the “deep” water column B (WCB) Thaumarchaeota . These ecotypes show a strong depth distribution, with WCB dominant at ≥ 200 m depth and WCA most abundant in surface (5–100 m) waters. The NP ecotype was found throughout the water column with the highest abundance in summer, and was the only ecotype showing a correlation with measured nitrification rates. We also found three abundant taxa related to Nitrospina —the major nitrite‐oxidizing bacteria in the ocean; these showed clear connections to each of the three Thaumarchaeota ecotypes, suggesting a specific relationship between both steps of nitrification. Our results support the importance of ecotype‐based analysis of Thaumarchaeota and show that their abundance and distribution are controlled based on their water column position, with a distinct shift at 50 m between euphotic and mesopelagic depths.
Thaumarchaeota
Ecotype
Mesopelagic zone
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Microorganisms play fundamental roles in the ecosystem of the Gulf of Mexico (GOM), yet their vertical distributions along the depth continuum of water column are not well known. In this study, we presented the 16S rDNA sequences and lipid profiles in the context of water chemistry to characterize the archaeal community structure above a gas hydrate mound (MC 118) in GOM. Our results showed that all archaeal sequences were related to unknown species of Crenarchaeota or Euryarchaeota. Phylogenetically, group II –β Euryarchaeota dominated the surface water and mid-depth (400-m) water (74% and 58% of total archaeal species, respectively) whereas the marine group I-γ Crenarchaeota dominated the bottom (869 m) water (61% of total archaeal species). Estimates of the Shannon index showed the highest diversity of planktonic Archaea at the 400 m depth. Glycerol dialkyl glycerol tetraether (GDGT) lipids were detected from the 400- and 869-m depths only and characterized by relatively high abundances of GDGT-5 (crenarchaeol) and GDGT-0. Our studies suggested a possible zonation of archaeal community in the water column, which did not seem to be affected by the possible venting of hydrocarbons from the hydrate location in GOM.
Crenarchaeota
Euryarchaeota
Thaumarchaeota
Clathrate hydrate
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Thaumarchaeota are one of the most abundant groups of Archaea in the marine water column. Their membrane consists of isoprenoid glycerol dibiphytanyl glycerol tetraethers (GDGTs) which are applied in the widely used TEX86 proxy to reconstruct past sea surface temperatures (SSTs). However, in some specific marine systems, such as the Mediterranean Sea, core-top TEX86-derived temperatures do not seem to reflect annual mean SSTs. This has been attributed to contributions of deep-water dwelling Thaumarchaeota. Here, we investigate the potential causes of this bias by studying both the archaeal diversity as well as the intact polar lipid (IPL) GDGT composition in the Mediterranean water column by a combined 16S rRNA gene amplicon sequencing and a lipidomic approach on suspended particulate matter (SPM) at different water depths. The archaeal distribution showed a dominance of archaea other than Thaumarchaeota, i.e. Marine Euryarchaeota group II and III in the upper epipelagic waters (0–100 m deep), while Thaumarchaeota (Marine group I; MGI) dominated the subsurface and the deeper waters. This shift in the archaeal community composition coincided with a decrease in IPL GDGT-0 and increase of IPL crenarchaeol. The ratio of GDGT-2/GDGT-3 increased with water depth, but values were lower than observed in deep marine waters of some other regions. The increase of the GDGT-2/GDGT-3 ratio coincided with the high relative abundance of deep-water MGI, which may be linked to the high temperature and salinity found in specific water masses of the Mediterranean Sea. We conclude that these particularities of the Mediterranean Sea are responsible for the overestimated SST based on TEX86.
Thaumarchaeota
Dominance (genetics)
Mesopelagic zone
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The annual dynamics of three different ammonia-oxidizing archaea (AOA) ecotypes (amoA gene) and of the SAGMGC-1 (Nitrosotalea-like aquatic Thaumarchaeota) group (16S rRNA gene) were studied by newly designed specific primers and quantitative polymerase chain reaction analysis in a deep oligotrophic high mountain lake (Lake Redon, Limnological Observatory of the Pyrenees, Spain). We observed segregated distributions of the main AOA populations, peaking separately in time and space, and under different ammonia concentrations and irradiance conditions. Strong positive correlation in gene abundances was found along the annual survey between 16S rRNA SAGMAGC-1 and one of the amoA ecotypes suggesting the potential for ammonia oxidation in the freshwater SAGMAGC-1 clade. We also observed dominance of Nitrosotalea-like ecotypes over Nitrosopumilus-like (Marine Group 1.1a) and not the same annual dynamics for the two thaumarchaeotal clades. The fine scale segregation in space and time of the different AOA ecotypes indicated the presence of phylogenetically close but ecologically segregated AOA species specifically adapted to specific environmental conditions. It remains to be elucidated what would be such environmental drivers.
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Thaumarchaeota
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Abstract Thaumarchaeota are among the most abundant prokaryotes in the ocean, playing important roles in carbon and nitrogen cycling. Marine Thaumarchaeota ecotypes exhibit depth‐related diversification and seasonal changes. However, transcriptomic activities concerning niche partitioning among thaumarchaeal ecotypes remain unclear. Here, we examined the variations in the distribution and transcriptomic activity of marine Thaumarchaeota ecotypes. Three primary ecotypes were identified: a Nitrosopumilus ‐like clade; a Nitrosopelagicus ‐like water column A (WCA) clade, thriving in epipelagic water; and a water column B (WCB) clade, dominant in deep water. Depth‐related partitioning of the three ecotypes and the seasonal variability of the WCA and WCB ecotypes were observed. Nutrient concentrations, chlorophyll α and salinity were the primary environmental factors. The relative abundance of the WCA ecotype and its transcript abundance of amoA gene were positively correlated with chlorophyll α and salinity, while the WCB ecotype was positively correlated with nitrate and phosphate. Based on high‐quality metagenome‐assembled genomes, transcriptomic analysis revealed that the three ecotypes exhibited various co‐occurring expression patterns of the elemental cycling genes in the nitrogen, carbon, phosphorus, and sulfur cycles. Our results provide transcriptomic evidence of the niche differentiation of marine Thaumarchaeota ecotypes, highlighting the diverse roles of ecotypes and WCA subclades in biogeochemical cycles.
Ecotype
Thaumarchaeota
Niche differentiation
Biogeochemical Cycle
Nitrogen Cycle
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Abstract Concentrated seabed deposits of polymetallic nodules, which are rich in economically valuable metals (e.g., copper, nickel, cobalt, manganese), occur over vast areas of the abyssal Pacific Ocean floor. Little is currently known about the diversity of microorganisms inhabiting abyssal habitats. In this study, sediment, nodule, and water column samples were collected from the Clarion‐Clipperton Zone of the Eastern North Pacific. The diversities of prokaryote and microeukaryote communities associated with these habitats were examined. Microbial community composition and diversity varied with habitat type, water column depth, and sediment horizon. Thaumarchaeota were relatively enriched in the sediments and nodules compared to the water column, whereas Gammaproteobacteria were the most abundant sequences associated with nodules. Among the Eukaryota, rRNA genes belonging to the Cryptomonadales were relatively most abundant among organisms associated with nodules, whereas rRNA gene sequences deriving from members of the Alveolata were relatively enriched in sediments and the water column. Nine operational taxonomic unit ( OTU )s were identified that occur in all nodules in this dataset, as well as all nodules found in a study 3000–9000 km from our site. Microbial communities in the sediments had the highest diversity, followed by nodules, and then by the water column with <1/3 the number of OTU s as in the sediments.
Thaumarchaeota
Operational taxonomic unit
Abyssal zone
Abyssal plain
Nodule (geology)
Seabed
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Viral and prokaryotic abundance, production and diversity were determined throughout the water column of the subtropical Atlantic Ocean to assess potential variations in the relation between viruses and prokaryotes. Prokaryotic abundance and heterotrophic activity decreased by one and three orders of magnitude, respectively, from the epi- to the abyssopelagic layer. Although the lytic viral production (VP) decreased with depth, lysogenic VP was variable throughout the water column and did not show any trend with depth. The bacterial, archaeal and viral community composition were depth-stratified as determined by the automated ribosomal intergenic spacer analysis, terminal-restriction fragment length polymorphism and randomly amplified polymorphic DNA-PCR, respectively. Generally, the number of operational taxonomic units (OTUs) did not reveal consistent trends throughout the water column. Viral and prokaryotic abundance were strongly related to heterotrophic prokaryotic production, suggesting similar linkage strength between the viral and prokaryotic communities from the lower epi- to the abyssopelagic layer in the Atlantic Ocean. Strikingly, the prokaryotic and viral parameters exhibited a similar variability throughout the water column down to the abyssopelagic layers, suggesting that the dark ocean is as dynamic a system as is the lower epipelagic layer. It also indicates that viruses are apparently having a similar role for prokaryotic mortality in the dark oceanic realm as in surface waters. The more than twofold increase in bacterial OTUs from 2750 m depth to >5000 m depth and the concurrent decrease in viral OTUs, however, suggests that viruses might exhibit a wider host range in deep waters than in surface waters.
Thaumarchaeota
Prochlorococcus
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Water column data from CTD casts along the East Siberian Arctic Shelf on R/V Oden during 2011 (ESAS Water Column Methane project) For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/660543
CTD
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Thaumarchaeota
Prochlorococcus
Lysogenic cycle
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Citations (57)