To test the hypothesis that different drivers shape the diversity and biogeography of the total and active bacterial community, we examined the bacterial community composition along two transects, one from the inner Pearl River estuary to the open waters of the South China Sea (SCS) and the other from the Luzon Strait to the SCS basin, using 454 pyrosequencing of the 16S rRNA and 16S rRNA gene (V1-3 regions) and thereby characterizing the active and total bacterial community, respectively. The diversity and biogeographic patterns differed substantially between the active and total bacterial communities. Although the composition of both the total and active bacterial community was strongly correlated with environmental factors and weakly correlated with geographic distance, the active bacterial community displayed higher environmental sensitivity than the total community and particularly a greater distance effect largely caused by the active assemblage from deep waters. The 16S rRNA vs. rDNA relationships indicated that the active bacteria were low in relative abundance in the SCS. This might be due to a high competition between active bacterial taxa as indicated by our community network models. Based on these analyses, we speculate that high competition could cause some dispersal limitation of the active bacterial community resulting in a distinct distance-decay relationship. Altogether, our results indicated that the biogeographic distribution of bacteria in the SCS is the result of both environmental control and distance decay.
Heterotrophic prokaryotes express extracellular hydrolytic enzymes to cleave large organic molecules before taking up the hydrolyzed products. According to foraging theory, extracellular enzymes should be cell associated in dilute systems such as deep sea habitats, but secreted into the surrounding medium in diffusion-limited systems. However, extracellular enzymes in the deep sea are found mainly dissolved in ambient water rather than cell associated. In order to resolve this paradox, we conducted a global survey of peptidases and carbohydrate-active enzymes (CAZymes), two key enzyme groups initiating organic matter assimilation, in an integrated metagenomics, metatranscriptomics, and metaproteomics approach. The abundance, percentage, and diversity of genes encoding secretory processes, i.e., dissolved enzymes, consistently increased from epipelagic to bathypelagic waters, indicating that organic matter cleavage, and hence prokaryotic metabolism, is mediated mainly by particle-associated prokaryotes releasing their extracellular enzymes into diffusion-limited particles in the bathypelagic realm.
Ammonia oxidation to nitrite and its subsequent oxidation to nitrate provides energy to the two populations of nitrifying chemoautotrophs in the energy-starved dark ocean, driving a coupling between reduced inorganic nitrogen (N) pools and production of new organic carbon (C) in the dark ocean. However, the relationship between the flux of new C production and the fluxes of N of the two steps of oxidation remains unclear. Here, we show that, despite orders-of-magnitude difference in cell abundances between ammonia oxidizers and nitrite oxidizers, the two populations sustain similar bulk N-oxidation rates throughout the deep waters with similarly high affinities for ammonia and nitrite under increasing substrate limitation, thus maintaining overall homeostasis in the oceanic nitrification pathway. Our observations confirm the theoretical predictions of a redox-informed ecosystem model. Using balances from this model, we suggest that consistently low ammonia and nitrite concentrations are maintained when the two populations have similarly high substrate affinities and their loss rates are proportional to their maximum growth rates. The stoichiometric relations between the fluxes of C and N indicate a threefold to fourfold higher C-fixation efficiency per mole of N oxidized by ammonia oxidizers compared to nitrite oxidizers due to nearly identical apparent energetic requirements for C fixation of the two populations. We estimate that the rate of chemoautotrophic C fixation amounts to ∼1 × 1013to ∼2 × 1013mol of C per year globally through the flux of ∼1 × 1014to ∼2 × 1014mol of N per year of the two steps of oxidation throughout the dark ocean.
The South China Sea (SCS) is an oligotrophic subtropical marginal ocean with a deep basin and a permanently stratified central gyre. Upwelling and nitrogen fixation provide new nitrogen for primary production in the SCS. This study was aimed at an investigation of phylogenetic diversity and quantification of the diazotroph community in the SCS deep basin, which is characterized by frequent mesoscale eddies. The diazotroph community had a relatively low diversity but a distinct spatial heterogeneity of diversity in the SCS deep basin. The potential for nitrogen fixation consistently occurred during cyclonic eddies, although upwelling of nutrient-replete deep water might have alleviated nitrogen limitation in the SCS. However, diazotrophic proteobacteria were dominant, but neither Trichodesmium nor heterocystous cyanobacterial diatom symbionts. Quantitative PCR analysis using probe-primer sets developed in this study revealed that the nif H gene of the two dominant alpha- and gammaproteobacterial groups was at the highest abundance (up to 10(4) to 10(5) copies L(-1) ). Trichodesmium thiebautii was detected with an average density of 10(2) trichomes L(-1) in the euphotic waters, while Richelia intracellularis was observed sporadically under the microscope. The unicellular cyanobacterial groups A and B were not detected in our libraries. Our results suggested that diazotrophic proteobacteria were significant components potentially contributing to nitrogen fixation in this oligotrophic marginal ocean ecosystem.
To determine microbial community composition, community spatial structure and possible key microbial processes in the shallow-sea hydrothermal vent systems off NE Taiwan’s coast, we examined the bacterial and archaeal communities of four samples collected from the water column extending over a redoxocline gradient of a yellow and four from a white hydrothermal vent. Ribosomal tag pyrosequencing based on DNA and RNA showed statistically significant differences between the bacterial and archaeal communities of the different hydrothermal plumes. The bacterial and archaeal communities from the white hydrothermal plume were dominated by sulfur-reducing Nautilia and Thermococcus, whereas the yellow hydrothermal plume and the surface water were dominated by sulfide-oxidizing Thiomicrospira and Euryarchaeota Marine Group II, respectively. Canonical correspondence analyses indicate that methane (CH4) concentration was the only statistically significant variable that explains all community cluster patterns. However, the results of pyrosequencing showed an essential absence of methanogens and methanotrophs at the two vent fields, suggesting that CH4 was less tied to microbial processes in this shallow-sea hydrothermal system. We speculated that mixing between hydrothermal fluids and the sea or meteoric water leads to distinctly different CH4 concentrations and redox niches between the yellow and white vents, consequently influencing the distribution patterns of the free-living Bacteria and Archaea. We concluded that sulfur-reducing and sulfide-oxidizing chemolithoautotrophs accounted for most of the primary biomass synthesis and that microbial sulfur metabolism fueled microbial energy flow and element cycling in the shallow hydrothermal systems off the coast of NE Taiwan.
Background Most of the research on the cycling of carbon in the open-ocean has focused on heterotrophic prokaryotes and eukaryotic phytoplankton, but the role of pelagic fungi remains largely enigmatic. Methods Here, we performed a global-ocean multi-omics analysis of all pelagic fungal carbohydrate-active enzymes (CAZymes), key enzymes in the carbon cycling. We studied the occurrence, expression, diversity, functional classification, and taxonomic affiliation of the genes encoding all pelagic fungal CAZymes from the epi- and mesopelagic realm. Results Pelagic fungi are active in carbohydrate degradation as indicated by a high ratio of CAZymes transcripts per gene. Dothideomycetes in epipelagic and the Leotiomycetes in mesopelagic waters (both from the phylum Ascomycota) are the main pelagic fungi responsible for carbohydrate degradation in the ocean. The abundance, expression, and diversity of fungal CAZymes were higher in the mesopelagic than in the epipelagic waters, in contrast to the distribution pattern of prokaryotic CAZymes. Conclusions Our results reveal a widespread utilization of different types of CAZymes by pelagic fungi, uncovering an active and hitherto largely unexplored participation of fungi in the pelagic C cycling, where pelagic prokaryotes and fungi occupy different ecological niches, and fungi becoming relatively more important with depth.
Alkaline phosphatase (APase) is one of the marine enzymes used by oceanic microbes to obtain inorganic phosphorus (Pi) from dissolved organic phosphorus to overcome P-limitation. Marine APase is generally recognized to perform P-monoesterase activity. Here we integrated a biochemical characterization of a specific APase enzyme, examination of global ocean databases, and field measurements, to study the type and relevance of marine APase promiscuity. We performed an in silico mining of phoA homologs, followed by de novo synthesis and heterologous expression in E. coli of the full-length gene from Alteromonas mediterranea, resulting in a recombinant PhoA. A global analysis using the TARA Oceans, Malaspina and other metagenomic databases confirmed the predicted widespread distribution of the gene encoding the targeted PhoA in all oceanic basins throughout the water column. Kinetic assays with the purified PhoA enzyme revealed that this enzyme exhibits not only the predicted P-monoester activity, but also P-diesterase, P-triesterase and sulfatase activity as a result of a promiscuous behavior. Among all activities, P-monoester bond hydrolysis exhibited the highest catalytic activity of APase despite its lower affinity for phosphate monoesters. APase is highly efficient as a P-monoesterase at high substrate concentrations, whereas promiscuous activities of APase, like diesterase, triesterase, and sulfatase activities are more efficient at low substrate concentrations. Strong similarities were observed between the monoesterase:diesterase ratio of the purified PhoA protein in the laboratory and in natural seawater. Thus, our results reveal enzyme promiscuity of APase playing potentially an important role in the marine phosphorus cycle.
Shallow-water hydrothermal vent ecosystems are distinctly different from deep-sea vents, as other than geothermal, sunlight is one of their primary sources of energy, so their resulting microbial communities differ to some extent. Yet compared with deep-sea systems, less is known about the active microbial community in shallow-water ecosystems. Thus, we studied the community compositions, their metabolic pathways, and possible coupling of microbially driven biogeochemical cycles in a shallow-water hydrothermal vent system off Kueishantao Islet, Taiwan, using high-throughput 16S rRNA sequences and metatranscriptome analyses. Gammaproteobacteria and Epsilonbacteraeota were the major active bacterial groups in the 16S rRNA libraries and the metatranscriptomes, and involved in the carbon, sulfur, and nitrogen metabolic pathways. As core players, Thiomicrospira, Thiomicrorhabdus, Thiothrix, Sulfurovum, and Arcobacter derived energy from the oxidation of reduced sulfur compounds and fixed dissolved inorganic carbon (DIC) by the Calvin-Benson-Bassham (CBB) or reverse tricarboxylic acid cycles. Sox-dependent and reverse sulfate reduction were the main pathways of energy generation, and probably coupled to denitrification by providing electrons to nitrate and nitrite. Sulfur-reducing Nautiliaceae members, accounting for a small proportion in the community, obtained energy by the oxidation of hydrogen, which also supplies metabolic energy for some sulfur-oxidizing bacteria. In addition, ammonia and nitrite oxidation is another type of energy generation in this hydrothermal system, with marker gene sequences belonging to Thaumarchaeota/Crenarchaeota and Nitrospina, respectively, and ammonia and nitrite oxidation was likely coupled to denitrification by providing substrate for nitrate and nitrite reduction to nitric oxide. Moreover, unlike the deep-sea systems, cyanobacteria may also actively participate in major metabolic pathways. This study helps us to better understand biogeochemical processes mediated by microorganisms and possible coupling of the carbon, sulfur, and nitrogen cycles in these unique ecosystems.
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