Size-fractionated microbiome observed during an eight-month long sampling in Jiaozhou Bay and the Yellow Sea.

Jiaozhou Bay is a typical semi-enclosed bay with a temperate climate imposed by strong anthropogenic influence. To investigate microbial biodiversity and ecosystem services in this highly dynamic coastal environment, we conducted a monthly microbial survey spanning eight months at two stations in the bay and the open Yellow Sea starting in April 2015. This report provides a comprehensive inventory of amplicon sequences and environmental microbial genomes from this survey. In total, 2,543 amplicon sequence variants were obtained with monthly relative abundance profiles in three size fractions (>2.7 µm, 2.7-0.7 µm, and 0.7-0.22 µm). Shotgun metagenomes yielded 915 high-quality metagenome-assembled genomes with ≥50% completeness and ≤5% contamination. These environmental genomes comprise 27 bacterial and 5 archaeal phyla. We expect this comprehensive dataset will facilitate a better understanding of coastal microbial ecology.

A Novel Approach to Characterize the Lipidome of Marine Archaeon Nitrosopumilus maritimus by Ion Mobility Mass Spectrometry.

Archaea are differentiated from the other two domains of life by their biomolecular characteristics. One such characteristic is the unique structure and composition of their lipids. Characterization of the whole set of lipids in a biological system (the lipidome) remains technologically challenging. This is because the lipidome is innately complex, and not all lipid species are extractable, separable, or ionizable by a single analytical method. Furthermore, lipids are structurally and chemically diverse. Many lipids are isobaric or isomeric and often indistinguishable by the measurement of mass or even their fragmentation spectra. Here we developed a novel analytical protocol based on liquid chromatography ion mobility mass spectrometry to enhance the coverage of the lipidome and characterize the conformations of archaeal lipids by their collision cross-sections (CCSs). The measurements of ion mobility revealed the gas-phase ion chemistry of representative archaeal lipids and provided further insights into their attributions to the adaptability of archaea to environmental stresses. A comprehensive characterization of the lipidome of mesophilic marine thaumarchaeon, Nitrosopumilus maritimus (strain SCM1) revealed potentially an unreported phosphate- and sulfate-containing lipid candidate by negative ionization analysis. It was the first time that experimentally derived CCS values of archaeal lipids were reported. Discrimination of crenarchaeol and its proposed stereoisomer was, however, not achieved with the resolving power of the SYNAPT G2 ion mobility system, and a high-resolution ion mobility system may be required for future work. Structural and spectral libraries of archaeal lipids were constructed in non-vendor-specific formats and are being made available to the community to promote research of Archaea by lipidomics.

Vertical Stratification of Dissolved Organic Matter Linked to Distinct Microbial Communities in Subtropic Estuarine Sediments.

Dissolved organic matter (DOM) provides carbon substrates and energy sources for sediment microbes driving benthic biogeochemical processes. The interactions between microbes and DOM are dynamic and complex and require the understanding based on fine-scale microbial community and physicochemical profiling. In this study, we characterized the porewater DOM composition in a 300-cm sediment core from the Pearl River estuary, China, and examined the interactions between DOM and archaeal and bacterial communities. DOM composition were highly stratified and associated with changing microbial communities. Compared to bacteria, the amplicon sequence variants of archaea showed significant Pearson correlations (r ≥ 0.65, P < 0.01) with DOM molecules of low H/C ratios, high C number and double bond equivalents, indicating that the distribution of archaea was closely correlated to recalcitrant DOM while bacteria were associated with relatively labile compounds. This was supported by the presence of auxiliary enzyme families essential for lignin degradation and bcrABCD, UbiX genes for anaerobic aromatic reduction in metagenome-assembled genomes of Bathyarchaeia. Our study demonstrates that niche differentiation between benthic bacteria and archaea may have important consequences in carbon metabolism, particularly for the transformation of recalcitrant organic carbon that may be predominant in aged marine sediments.

Characterization of the Exometabolome of Nitrosopumilus maritimus SCM1 by Liquid Chromatography-Ion Mobility Mass Spectrometry.

Marine Thaumarchaeota (formerly known as the marine group I archaea) have received much research interest in recent years since these chemolithoautotrophic organisms are abundant in the subsurface ocean and oxidize ammonium to nitrite, which makes them a major contributor to the marine carbon and nitrogen cycles. However, few studies have investigated the chemical composition of their exometabolome and their contributions to the pool of dissolved organic matter (DOM) in seawater. This study exploits the recent advances in ion mobility mass spectrometry (IM-MS) and integrates this instrumental capability with bioinformatics to reassess the exometabolome of a model ammonia-oxidizing archaeon, Nitrosopumilus maritimus strain SCM1. Our method has several advantages over the conventional approach using an Orbitrap or ion cyclotron resonance mass analyzer and allows assignments or annotations of spectral features to known metabolites confidently and indiscriminately, as well as distinction of biological molecules from background organics. Consistent with the results of a previous report, the SPE-extracted exometabolome of N. maritimus is dominated by biologically active nitrogen-containing metabolites, in addition to peptides secreted extracellularly. Cobalamin and associated intermediates, including α-ribazole and α-ribazole 5'-phosphate, are major components of the SPE-extracted exometabolome of N. maritimus. This supports the proposition that Thaumarchaeota have the capacity of de novo biosynthesizing cobalamin. Other biologically significant metabolites, such as agmatidine and medicagenate, predicted by genome screening are also detected, which indicates that Thaumarchaeota have remarkable metabolic potentials, underlining their importance in driving elemental cycles critical to biological processes in the ocean.

The Evolution Pathway of Ammonia-Oxidizing Archaea Shaped by Major Geological Events.

Primordial nitrification processes have been studied extensively using geochemical approaches, but the biological origination of nitrification remains unclear. Ammonia-oxidizing archaea (AOA) are widely distributed nitrifiers and implement the rate-limiting step in nitrification. They are hypothesized to have been important players in the global nitrogen cycle in Earth's early history. We performed systematic phylogenomic and marker gene analyses to elucidate the diversification timeline of AOA evolution. Our results suggested that the AOA ancestor experienced terrestrial geothermal environments at ∼1,165 Ma (1,928-880 Ma), and gradually evolved into mesophilic soil at ∼652 Ma (767-554 Ma) before diversifying into marine settings at ∼509 Ma (629-412 Ma) and later into shallow and deep oceans, respectively. Corroborated by geochemical evidence and modeling, the timing of key diversification nodes can be linked to the global magmatism and glaciation associated with the assembly and breakup of the supercontinent Rodinia, and the later oxygenation of the deep ocean. Results of this integrated study shed light on the geological forces that may have shaped the evolutionary pathways of the AOA, which played an important role in the ancient global nitrogen cycle.

Interactions Between Marine Group II Archaea and Phytoplankton Revealed by Population Correlations in the Northern Coast of South China Sea.

Marine Group II (MGII) archaea (Poseidoniales) are the most abundant surface marine planktonic archaea and are widely distributed in both coastal and pelagic waters. The factors affecting their distribution and activity are poorly understood. MGII archaea have the metabolic potential to utilize algae-derived organic matter and are frequently observed in high abundance during or following phytoplankton blooms, suggesting that they are key players of the marine food web. In this study, we studied interactions between MGII archaea and the diverse taxa of phytoplankton in the northern coast of South China Sea. Non-metric multidimensional scaling and cluster analyses demonstrated distinct MGII community patterns in the Pearl River plume (PRP) and the open regions of the northern South China Sea (ONSCS), with MGIIb dominating the former and MGIIa and MGIIb showing remarkable variations in the latter for the same sampling season. Nevertheless, positive correlations (Pearson correlation: R > 0.8 and P < 0.01) in absolute abundances of ribosomal RNA (rRNA)-derived complementary DNA and rRNA genes from network analyses were found between MGII archaea and phytoplankton (cyanobacteria, haptophytes, and stramenopiles in both PRP and ONSCS) among different particle size fractions, indicating their intrinsic relationships under changing environmental conditions. The results of this study may shed light on the multiple interactions between co-existing species in the micro-niches of different oceanic regions.

Contrasting bacterial and archaeal distributions reflecting different geochemical processes in a sediment core from the Pearl River Estuary.

Microbial community structure and metabolic activities have profound impacts on biogeochemical processes in marine sediments. Functional bacteria such as nitrate- and sulfate-reducing bacteria respond to redox gradients by coupling specific reactions amenable to relevant energy metabolisms. However, similar functional patterns have not been observed for sedimentary archaea (except for anaerobic methanotrophs and methanogens). We coupled taxonomic composition with comprehensive geochemical species to investigate the participation of distinct bacteria and archaea in sedimentary geochemical cycles in a sediment core (300 cm) from Pearl River Estuary (PRE). Geochemical properties (NO3-, dissolved Mn and Fe, SO42+, NH4+; dissolved inorganic carbon (DIC), δ13CDIC, dissolved organic carbon (DOC), total organic carbon (TOC), δ13CTOC, and fluorescent dissolved organic matter (FDOM)) exhibited strong depth variability of different trends. Bacterial 16S rRNA- and dsrB gene abundance decreased sharply with depth while archaeal and bathyarchaeotal 16S rRNA gene copies were relatively constant. This resulted in an increase in relative abundance of archaea from surface (11.6%) to bottom (42.8%). Network analysis showed that bacterial groups of Desulfobacterales, Syntrophobacterales and Gammaproteobacteria were significantly (P < 0.0001) associated with SO42- and dissolved Mn while archaeal groups of Bathyarchaeota, Group C3 and Marine Benthic Group D (MBGD) showed close positive correlations (P < 0.0001) with NH4+, δ13CTOC values and humic-like FDOM. Our study suggested that these bacterial groups dominated in redox processes relevant to sulfate or metal oxides, while the archaeal groups are more like to degrade recalcitrant organic compounds in anaerobic sediments.

Stratification of dissolved organic matter in the upper 2000 m water column at the Mariana Trench.

Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) and absorbance spectroscopy were utilized to investigate the molecular composition of marine dissolved organic matter (DOM) from the upper 2000 m water column at the Mariana Trench. Molecular indices, calculated based on the relative abundance of 4699 formulas assigned from FT-ICR MS data, showed depth stratification. The degradation index (IDEG) varied from 0.610 to 0.663 (0.645 ±â€¯0.014) in the surface layer to 0.668-0.754 (0.722 ±â€¯0.021) in the deep ocean (below 500 m), indicating that the DOM in the deep layer was more refractory than that of the surface layer. This was confirmed by an increase of modified aromaticity index (AImod) from 0.196 to 0.207 (0.200 ±â€¯0.003) in the surface layer to 0.213-0.225 (0.220 ±â€¯0.003) at depth. Multivariate analysis based on both bulk molecular parameters and relative abundance of individual formulas showed that the molecular composition of DOM was highly stratified and could be well separated into three groups: the upper layer (5-75 m), the middle layer (200 m) and the deep layer (500-2000 m). In addition, surface-enriched and deep-enriched formulas were identified based on Spearman correlation between relative abundance of individual formulas and depth. The surface-enriched formulas were characterized by higher H/C and lower AImod, while deep-enriched formulas showed lower H/C and higher AImod. Variations in AImod and H/C for these formulas indicated that extracellular release (mainly from primary production) and photochemical processes strongly affected the DOM composition in euphotic zone, while microbial processes likely exerted a tremendous influence on the DOM composition at all depths. Moreover, strong correlations between spectroscopic indices (a325, S275-295 and S280-400) and FT- ICR MS derived proxies indicated these two approaches can be integrated to provide valuable information on the molecular characterization of open ocean DOM.