New perspectives in benthic deep-sea microbial ecology (original) (raw)
Related papers
Microbial diversity in the deep sea and the underexplored "rare biosphere
Proceedings of the …, 2006
The evolution of marine microbes over billions of years predicts that the composition of microbial communities should be much greater than the published estimates of a few thousand distinct kinds of microbes per liter of seawater. By adopting a massively parallel tag sequencing strategy, we show that bacterial communities of deep water masses of the North Atlantic and diffuse flow hydrothermal vents are one to two orders of magnitude more complex than previously reported for any microbial environment. A relatively small number of different populations dominate all samples, but thousands of low-abundance populations account for most of the observed phylogenetic diversity. This ''rare biosphere'' is very ancient and may represent a nearly inexhaustible source of genomic innovation. Members of the rare biosphere are highly divergent from each other and, at different times in earth's history, may have had a profound impact on shaping planetary processes.
Marine Drugs, 2013
Although emerging evidence indicates that deep-sea water contains an untapped reservoir of high metabolic and genetic diversity, this realm has not been studied well compared with surface sea water. The study provided the first integrated meta-genomic and -transcriptomic analysis of the microbial communities in deep-sea water of North Pacific Ocean. DNA/RNA amplifications and simultaneous metagenomic and metatranscriptomic analyses were employed to discover information concerning deep-sea microbial communities from four different deep-sea sites ranging from the mesopelagic to pelagic ocean. Within the prokaryotic community, bacteria is absolutely dominant (~90%) over archaea in both metagenomic and metatranscriptomic data pools. The emergence of archaeal phyla Crenarchaeota, Euryarchaeota, Thaumarchaeota, bacterial phyla Actinobacteria, Firmicutes, sub-phyla Betaproteobacteria, Deltaproteobacteria, and Gammaproteobacteria, and the decrease of bacterial phyla Bacteroidetes and Alphaproteobacteria are the main composition changes of prokaryotic communities in the deep-sea water, when compared with the reference Global Ocean Sampling Expedition (GOS) surface water. Photosynthetic Cyanobacteria exist in all four metagenomic libraries and two metatranscriptomic libraries. In Eukaryota community, decreased abundance of fungi and algae in deep sea was observed. RNA/DNA ratio was employed as an index to show metabolic activity strength of microbes in deep sea. Functional analysis indicated that deep-sea microbes are leading a defensive lifestyle.
2014
Author(s): Leon-Zayas, Rosa Iris | Abstract: This dissertation presents the analyses of twenty-eight single amplified genomes (SAGs) distributed among four major phyla or candidate phyla of archaea and bacteria : Thaumarchaeota, Proteobacteria, Parcubacteria and Marinimicrobia. Samples were obtained from 8,219 m and 10, 908 m depth within the hadal ecosystems of the Puerto Rico Trench (PRT) and Challenger Deep (CHDE) portion of the Mariana Trench, respectively, and microbes associated with seawater, invertebrates and surficial sediments were sorted, amplified by multiple displacement amplification and sequenced using the HiSeq 2000 Illumina platform. Assembled and annotated genomes were analyzed and compared to genomes derived from closely related microbes from other habitats with the goal of understanding PRT and CHDE microbes' metabolic adaptations to deep-sea conditions. Four single amplified genomes (SAGs) were recovered from the PRT: PRT Nitrosopumilus, PRT SAR11, PRT Marin...
Aquatic Microbial Ecology
The deep-ocean interior contains the majority of microbes present on Earth. Most deep-sea microbes are concentrated in surface sediments, with abundances up to 4 orders of magnitude higher, per unit of volume, than in highly productive waters of the photic zone. To date, it has been shown that prokaryotic biomass largely dominates over all other biotic components, but the relative importance of Bacteria, Archaea and viruses to the global benthic biomass has not yet been quantified. Here, we report that the microbial abundance in the top 50 cm of deep-sea sediments of the world oceans is on the order of 1.5 ± 0.4 × 10 29. This is largely represented by viruses (9.8 ± 2.5 × 10 28), followed by Bacteria (3.5 ± 0.9 × 10 28 cells) and Archaea (1.4 ± 0.4 × 10 28 cells). The overall biomass in the top 50 cm of the deep-sea sediments is 1.7 ± 0.4 Pg C, largely represented by bacterial biomass (ca. 78%), followed by archaeal biomass (ca. 21%) and viruses (<1%). The bathymetric patterns of abundance and biomass of the 3 microbial components show differences: abundance and biomass of Bacteria decrease with increasing water depth, whereas those of Archaea and viruses remain constant. These results support the hypothesis that the role of Archaea and viruses could be more relevant in the deepest part of the ocean floor.
Metabolic Architecture of the Deep Ocean Microbiome
The deep sea, the largest compartment of the ocean, is an essential component of the Earth system, but the functional exploration of its microbial communities lags far behind that of other marine realms. Here we analyze 58 bathypelagic microbial metagenomes from the Atlantic, Indian, and Pacific Oceans in an unprecedented sampling effort from the Malaspina Global Expedition, to resolve the metabolic architecture of the deep ocean microbiome. The Malaspina Deep-Sea Gene Collection, 71% of which consists of novel genes, reveals a strong dichotomy between the functional traits of free-living and particle-attached microorganisms, and shows relatively patchy composition challenging the paradigm of a uniform dark ocean ecosystem. Metagenome Assembled Genomes uncovered 11 potential new phyla, establishing references for deep ocean microbial taxa, and revealed mixotrophy to be a widespread trophic strategy in the deep ocean. These results expand our understanding of the functional diversity...
Structure and function of the global ocean microbiome
Science, 2015
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.
Applied and Environmental Microbiology, 2009
The deep sea (water depth of >2,000 m) represents the largest biome on Earth. Yet relatively little is known about its microbial community's structure, function, and adaptation to the cold and deep biosphere. To provide further genomic insights into deep-sea planktonic microbes, we sequenced a total of ∼200 Mbp of a random whole-genome shotgun (WGS) library from a microbial community residing at a depth of 4,000 m at Station ALOHA in the Pacific Ocean and compared it to other available WGS sequence data from surface and deep waters. Our analyses indicated that the deep-sea lifestyle is likely facilitated by a collection of very subtle adaptations, as opposed to dramatic alterations of gene content or structure. These adaptations appear to include higher metabolic versatility and genomic plasticity to cope with the sparse and sporadic energy resources available, a preference for hydrophobic and smaller-volume amino acids in protein sequences, unique proteins not found in surfa...
Metaproteomic analysis decodes the trophic basis of microbes in the dark ocean
Research Square (Research Square), 2023
Microbes living in the dark ocean largely rely on the particulate organic matter (POM) input due the low bioavailability of deep-sea dissolved organic matter (DOM)1-3. Despite various POM injection mechanisms, coined as 'pumps'4-6, and dark inorganic carbon(DIC) xation7-9 are thought to fuel deepsea microbial community, the source, composition and regeneration pathway from POM to DOM remains unclear. Here using a metaproteomic approach targeting on the structure and function of microbial communities (including eukaryotes, bacteria, archaea and virus), we reveal a size-fractionated pattern in marine protein pool. We show that zooplankton produces three time more than algae to the protein fraction of deep-sea POM. Gammaproteobacteria exhibits high metabolic activity in POM assimilation and contributes 30% of bacterial biomass. Viral lysis on active Gammaproteobacteria further converts bacterial biomass into DOM, which constitutes 80% of protein fraction of DOM. The DIC xation mediated by nitri ers also bene ts from the urea released by zooplankton. These nding suggests that the POM and inorganic nutrient from zooplankton are of great importance in deep-sea carbon cycle, and the carbon delivery mechanism mediated by zooplankton, bacteria, archaea and viruses is intrinsically connected. Full Text Particulate organic matter (POM) and dissolved inorganic carbon (DIC) xation have been proposed as the main trophic basis for heterotrophic microbes in the dark ocean 1,7,8,10. However, the contribution of individual organismal groups to the dissolved organic matter (DOM) pool and the role of free-living versus particle-associated microbes in transforming DOM in the deep ocean, remains enigmatic 1-3. During the last decade, metagenomic and metatranscriptomic surveys revealed the structure and function of marine microorganisms 7,8,11-15 providing information on the metabolic potential of bacteria and archaea in the global ocean carbon cycle. However, the link between the genetic potential (metagenomics), the transcriptional response (metatranscriptomics) and the metabolic function (metaproteomics) is not well documented, especially in the deep ocean. Proteins are essential biomolecules for all living organisms. While their expression level is a direct response to the (micro)environment 16-18 , their abundance is also a measure of the contribution of individual populations to the total biomass in a speci c depth layer in the oceanic water column 19. We characterized the structure and function of marine microbial communities using a metaproteomics approach to assess the protein abundance of individual taxa, we also focused on microbial enzyme expression pro les to determine the links between organic matter supply and microbial activities. Protein pro les of the marine plankton community We collected metaproteomic samples between 5m and 4000m depth of the major ocean basins and three size-fractions (>0.8mm, 0.2-0.8mm, and <0.2mm) to cover eukaryotes, bacteria, archaea, and viruses (Fig. 1A, Extended Data Fig. 1A-C, supplementary dataset 1, see Methods). Metaproteomic analysis heavily relies on the completeness of sequence database, a well curated gene catalog from global scale metagenomic and metatranscriptomic surveys 11,12,14,15,20 will signi cantly improve the protein identi cation and functional pro ling in the metaproteome. Here we employed an optimized database construction strategy for robust protein identi cation 21. Metagenomic assembles from same sampling stations were combined to publically available metagenomics/metatranscriptomic assembles to obtain a full coverage of all organisms in the ocean (including eukaryotes, bacteria, archaea and virus) throughout the entire water column from global ocean expiditions 11,12,14,15,20. A two-step searching approach was implemented to minimize the high false discovery rate in protein identi cation caused by large database size 22. Searching against such comprehensive database covering marine micro-eukaryotes (79,577,878 sequences), prokaryotes (105,585,296 sequences) and viruses (1,501,235 sequences), we identi ed 234,550 protein entries (Extended Data Table 1, supplementary dataset 2, see Methods). Bacterial (156,187) and eukaryotic (55,494) sequences were highly abundant, followed by archaeal (7,163) and viral (6,213) sequences (Extended Data Table 2). More than 70% of the protein sequences were taxonomically classi ed at the class level and were also functionally annotated in at least one functional database (Extended Data Fig. 1D, E). While protein counts represent protein occurrence, peptide-spectrum matches (PSMs) are related to protein abundance. By investigating the relationship between taxonomic a liation and protein sequence attributes (protein counts, unique peptides and peptide-spectrum matches), our results, for the rst time, identi ed the major contributors to the marine protein pool. Bacteroidetes, Alpha-and Gamma-proteobacteria (especially Alteromonadales) from the Bacteria domain dominated the identi ed protein pool (Fig. 1A). Sequences from bacterial autotrophs such as Cyanobacteria and Thaumarchaea were also abundant. Interestingly, SAR11, despite their high abundance throughout the ocean 23 , contributed only marginally to the metaproteomic dataset (Fig. 1A). Sequences related to Myoviridae were the most abundant viral proteins. Eukaryotic proteins mainly originated from algae and zooplankton (Fig. 1A). Across kingdoms the analysis detected clear differences between the size-fractions and depth strata in the protein distribution pattern (Fig. 1B). For example, more than 45% of eukaryotic proteins were found in the >0.8mm fraction in the epipelagic realm, bacterial and archaeal proteins dominated the 0.2-0.8mm fraction throughout the water column and viral proteins were detected in the <0.2mm fraction. The functional annotations of sequences from each kingdom varied drastically (Fig. 1C). Bacterial proteins were involved in energy production and cellular metabolism, while eukaryotic proteins were mainly involved in protein synthesis and cytoskeleton interlinking. Functional assessment of the metaproteome was carried out using KEGG-orthologues (KOs) based analysis 24. Protein sequences were grouped into 3,817 KOs (supplementary dataset 3). The relative abundance of KOs revealed that although the sample size and the number of detected KOs were different between "omics" dataset (Extended Data Fig. 2A, B), KOs with high abundances in the metagenome and metatranscriptome were also highly abundant in the metaproteome (Extended Data Fig. 2C). The functional composition of the metaproteome, however, was signi cantly different (Fig. 2A, PERMANOVA, p<0.05) from the metagenome and metatranscriptome for both, the eukaryotic and prokaryotic community 11-13. Diversity analysis on KOs showed that the metaproteomics dataset had the lowest alpha-diversity but a high beta-diversity (Wilcoxon test, p<0.05, Fig. 2B, C). Clusters of size-fractions were found in the metagenomic and-transcriptomic dataset (Fig. 2A), as well as at the metaproteome level (Fig. 2D, PERMANOVA, p<0.05), although the metaproteomic samples were collected from disparate ocean regions (Extended Data Fig. 1A). The metaproteomic KO pro le in the >0.8mm size-fraction showed the
Going Deeper: Metagenome of a Hadopelagic Microbial Community
PLoS ONE, 2011
The paucity of sequence data from pelagic deep-ocean microbial assemblages has severely restricted molecular exploration of the largest biome on Earth. In this study, an analysis is presented of a large-scale 454-pyrosequencing metagenomic dataset from a hadopelagic environment from 6,000 m depth within the Puerto Rico Trench (PRT). A total of 145 Mbp of assembled sequence data was generated and compared to two pelagic deep ocean metagenomes and two representative surface seawater datasets from the Sargasso Sea. In a number of instances, all three deep metagenomes displayed similar trends, but were most magnified in the PRT, including enrichment in functions for two-component signal transduction mechanisms and transcriptional regulation. Overrepresented transporters in the PRT metagenome included outer membrane porins, diverse cation transporters, and di-and tri-carboxylate transporters that matched well with the prevailing catabolic processes such as butanoate, glyoxylate and dicarboxylate metabolism. A surprisingly high abundance of sulfatases for the degradation of sulfated polysaccharides were also present in the PRT. The most dramatic adaptational feature of the PRT microbes appears to be heavy metal resistance, as reflected in the large numbers of transporters present for their removal. As a complement to the metagenome approach, single-cell genomic techniques were utilized to generate partial whole-genome sequence data from four uncultivated cells from members of the dominant phyla within the PRT, Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes and Planctomycetes. The single-cell sequence data provided genomic context for many of the highly abundant functional attributes identified from the PRT metagenome, as well as recruiting heavily the PRT metagenomic sequence data compared to 172 available reference marine genomes. Through these multifaceted sequence approaches, new insights have been provided into the unique functional attributes present in microbes residing in a deeper layer of the ocean far removed from the more productive sun-drenched zones above.
Sedimentomics - Exploring the Microbial Treasures in Deep Marine Environments
Journal of Investigative Genomics, 2016
Advancements in metagenomics and related molecular approaches has allowed easy access to extreme and less explored vicinities over the globe, one of the best examples being the deep marine sediment microbial communities. Several recent investigations have provided access to high number of genomic and metagenomic datasets from circumnavigation in different water bodies that form a major portion of the Earth's surface area. And these microbes play a significant role in the biogeochemical cycles, biodegradation of hydrocarbons and most importantly help in elucidating the vast arena of antibiotics and antibiotic resistance that poses immense health risk to humans. Here, we summarize the advancements in deep sediment microbiome studies using the '-omic' technologies and the remarkable functional and community observations that have enriched the marine microbes' database in an extremely short span of time.