Microbes are dominant drivers of biogeochemical processes, yet drawing a global picture of functional diversity, microbial community structure, and their ecological determinants remains a grand challenge. We analyzed 7.2 terabases of metagenomic data from 243 Tara Oceans samples from 68 locations in epipelagic and mesopelagic waters across the globe to generate an ocean microbial reference gene catalog with >40 million nonredundant, mostly novel sequences from viruses, prokaryotes, and picoeukaryotes. Using 139 prokaryote-enriched samples, containing >35,000 species, we show vertical stratification with epipelagic community composition mostly driven by temperature rather than other environmental factors or geography. We identify ocean microbial core functionality and reveal that >73% of its abundance is shared with the human gut microbiome despite the physicochemical differences between these two ecosystems.
Sequencing of 16S rDNA polymerase chain reaction (PCR) amplicons is the most common approach for investigating environmental prokaryotic diversity, despite the known biases introduced during PCR. Here we show that 16S rDNA fragments derived from Illumina-sequenced environmental metagenomes (mi tags) are a powerful alternative to 16S rDNA amplicons for investigating the taxonomic diversity and structure of prokaryotic communities. As part of the Tara Oceans global expedition, marine plankton was sampled in three locations, resulting in 29 subsamples for which metagenomes were produced by shotgun Illumina sequencing (ca. 700 Gb). For comparative analyses, a subset of samples was also selected for Roche-454 sequencing using both shotgun (m454 tags; 13 metagenomes, ca. 2.4 Gb) and 16S rDNA amplicon (454 tags; ca. 0.075 Gb) approaches. Our results indicate that by overcoming PCR biases related to amplification and primer mismatch, mi tags may provide more realistic estimates of community richness and evenness than amplicon 454 tags. In addition, mi tags can capture expected beta diversity patterns. Using mi tags is now economically feasible given the dramatic reduction in high-throughput sequencing costs, having the advantage of retrieving simultaneously both taxonomic (Bacteria, Archaea and Eukarya) and functional information from the same microbial community.
Phytoplankton and heterotrophic prokaryotes are major components of the microbial food web and interact continuously: heterotrophic prokaryotes utilize the dissolved organic carbon derived from phytoplankton exudation or cell lysis (DOCp), and mineralization by heterotrophic prokaryotes provides inorganic nutrients for phytoplankton. For this reason, these communities are expected to be closely linked, although the study of the interactions between them is still a major challenge. Recent studies have presented interactions between phytoplankton and heterotrophic prokaryotes based on coexistence or covariation throughout a time-series. However, a real quantification of the carbon flow within these networks (defined as the interaction strength, IS) has not been achieved yet. This is critical to understand the selectivity degree of bacteria responding to specific algal DOCp. Here we used microautoradiography to quantify the preferences of the major heterotrophic prokaryote phylogenetic groups on DOC derived from several representative phytoplankton species, and expressed these preferences as an IS value. The distribution of the ISs was not random but rather skewed towards weak interactions, in a similar way as the distributions described for stable complex non-microbial ecosystems, indicating that there are some cases of high specificity on the use of specific algal DOCp by some bacterial groups, but weak interactions are more common and may be relevant as well. The variety of IS patterns observed supports the view that the vast range of different resources (different types of organic molecules) available in the sea selects and maintains the high levels of diversity described for marine bacterioplankton.
An understanding of the distribution of colored dissolved organic matter (CDOM) in the oceans and its role in the global carbon cycle requires a better knowledge of the colored materials produced and consumed by marine phytoplankton and bacteria. In this work, we examined the net uptake and release of CDOM by a natural bacterial community growing on DOM derived from four phytoplankton species cultured under axenic conditions. Fluorescent humic-like substances exuded by phytoplankton (excitation/emission [Ex/Em] wavelength, 310 nm/392 nm; Coble's peak M) were utilized by bacteria in different proportions depending on the phytoplankton species of origin. Furthermore, bacteria produced humic-like substances that fluoresce at an Ex/Em wavelength of 340 nm/440 nm (Coble's peak C). Differences were also observed in the Ex/Em wavelengths of the protein-like materials (Coble's peak T) produced by phytoplankton and bacteria. The induced fluorescent emission of CDOM produced by prokaryotes was an order of magnitude higher than that of CDOM produced by eukaryotes. We have also examined the final compositions of the bacterial communities growing on the exudates, which differed markedly depending on the phytoplankton species of origin. Alteromonas and Roseobacter were dominant during all the incubations on Chaetoceros sp. and Prorocentrum minimum exudates, respectively. Alteromonas was the dominant group growing on Skeletonema costatum exudates during the exponential growth phase, but it was replaced by Roseobacter afterwards. On Micromonas pusilla exudates, Roseobacter was replaced by Bacteroidetes after the exponential growth phase. Our work shows that fluorescence excitation-emission matrices of CDOM can be a helpful tool for the identification of microbial sources of DOM in the marine environment, but further studies are necessary to explore the association of particular bacterial groups with specific fluorophores.Colored dissolved organic matter (CDOM) is receiving increasing attention due to its important role in aquatic ecosystems. It regulates UV and visible light penetration in the water column, thus influencing primary productivity (2) and preventing cellular DNA damage (16,17). CDOM can also form complexes with metals, reducing the concentrations of free ions in seawater (28). In addition, changes in the optical properties of CDOM are suitable to trace microbial and photochemical degradation processes (34,45) and, more specifically, the in situ formation of biorefractory humic materials from bioavailable DOM (26). CDOM has also been the focus of remote sensing studies, given that the absorption spectrum of CDOM overlaps with that of chlorophyll a, affecting the satellite-derived estimates of phytoplankton biomass and activity in the oceans, especially in coastal areas (51).The fraction of CDOM that emits induced fluorescent light is called fluorescent dissolved organic matter (FDOM). Two main groups of fluorophores have been differentiated (9): protein-like substances, which fluoresce around an excitation/ emissio...
Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 104–105 genomes ml−1 for the samples from the photic zone and 102–103 genomes ml−1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.
Previsions of a warmer ocean as a consequence of climatic change point to a 2-68C temperature rise during this century in surface oceanic waters. Heterotrophic bacteria occupy the central position of the marine microbial food web, and their metabolic activity and interactions with other compartments within the web are regulated by temperature. In particular, key ecosystem processes like bacterial production (BP), respiration (BR), growth efficiency and bacterial -grazer trophic interactions are likely to change in a warmer ocean. Different approaches can be used to predict these changes. Here we combine evidence of the effects of temperature on these processes and interactions coming from laboratory experiments, space-for-time substitutions, long-term data from microbial observatories and theoretical predictions. Some of the evidence we gathered shows opposite trends to warming depending on the spatio-temporal scale of observation, and the complexity of the system under study. In particular, we show that warming (i) increases BR, (ii) increases bacterial losses to their grazers, and thus bacterial -grazer biomass flux within the microbial food web, (iii) increases BP if enough resources are available (as labile organic matter derived from phytoplankton excretion or lysis), and (iv) increases bacterial losses to grazing at lower rates than BP, and hence decreasing the proportion of production removed by grazers. As a consequence, bacterial abundance would also increase and reinforce the already dominant role of microbes in the carbon cycle of a warmer ocean.
Despite representing only a small fraction of the ocean's dissolved organic matter pool, dissolved free amino acids (DFAA) have high turnover rates and are major nitrogen and carbon sources for bacterioplankton. Both phytoplankton and bacterioplankton assimilate and release DFAA, but their consumption and production are difficult to quantify in nature due to their short residence times (min) as dissolved monomers. We segregated DFAA production by phytoplankton and bacterial consumption by measuring individual DFAA concentrations in four axenic phytoplankton cultures during the exponential growth phase, and also after 4 d incubations in the presence of a natural bacterioplankton community. The amounts and composition of the DFAA pool varied widely among phytoplankton species. The proportion of dissolved organic carbon attributed to DFAA varied among cultures. The picoeukaryotic prasinophyte, Micromonas pusilla, released higher amounts of DFAA than the other species tested (diatoms and dinoflagellate), especially alanine, which has been reported as the dominant individual DFAA in some oligotrophic environments. Community structure of heterotrophic prokaryotes responded to differences in the quality of organic matter released among microalgal species, with Roseobacterrelated bacteria responding strongly to exudate composition. Our results demonstrate the specificity of DFAA extracellular release among several algal species and their preferential uptake by members of bacterial communities.
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