Phytoplankton blooms characterize temperate ocean margin zones in spring. We investigated the bacterioplankton response to a diatom bloom in the North Sea and observed a dynamic succession of populations at genus-level resolution. Taxonomically distinct expressions of carbohydrate-active enzymes (transporters; in particular, TonB-dependent transporters) and phosphate acquisition strategies were found, indicating that distinct populations of Bacteroidetes, Gammaproteobacteria, and Alphaproteobacteria are specialized for successive decomposition of algal-derived organic matter. Our results suggest that algal substrate availability provided a series of ecological niches in which specialized populations could bloom. This reveals how planktonic species, despite their seemingly homogeneous habitat, can evade extinction by direct competition.
A process of global importance in carbon cycling is the remineralization of algae biomass by heterotrophic bacteria, most notably during massive marine algae blooms. Such blooms can trigger secondary blooms of planktonic bacteria that consist of swift successions of distinct bacterial clades, most prominently members of the Flavobacteriia, Gammaproteobacteria and the alphaproteobacterial Roseobacter clade. We investigated such successions during spring phytoplankton blooms in the southern North Sea (German Bight) for four consecutive years. Dense sampling and high-resolution taxonomic analyses allowed the detection of recurring patterns down to the genus level. Metagenome analyses also revealed recurrent patterns at the functional level, in particular with respect to algal polysaccharide degradation genes. We, therefore, hypothesize that even though there is substantial inter-annual variation between spring phytoplankton blooms, the accompanying succession of bacterial clades is largely governed by deterministic principles such as substrate-induced forcing.DOI: http://dx.doi.org/10.7554/eLife.11888.001
Symbioses between bacteria and eukaryotes are ubiquitous, yet our understanding of the interactions driving these associations is hampered by our inability to cultivate most host-associated microbes. Here, we used a metagenomic approach to describe four co-occurring symbionts from the marine oligochaete Olavius algarvensis, a worm lacking a mouth, gut, and nephridia. Shotgun sequencing and metabolic pathway reconstruction revealed that the symbionts are sulfur-oxidizing and sulfate-reducing bacteria, all of which are capable of carbon fixation, providing the host with multiple sources of nutrition. Molecular evidence for the uptake and recycling of worm waste products by the symbionts suggests how the worm could eliminate its excretory system, an adaptation unique among annelid worms. We propose a model which describes how the versatile metabolism within this symbiotic consortium provides the host with an optimal energy supply as it shuttles between the upper oxic and lower anoxic coastal sediments which it inhabits. 3 Symbiosis plays a major role in shaping the evolution and diversity of eukaryotic organisms 1 . Remarkably, only recently has there been an emerging recognition that most eukaryotic organisms are intimately associated with a complex community of beneficial microbes that are essential for their development, health, and interactions with the environment 2 . This renaissance in symbiosis research stems from advances in molecular approaches that have enabled the study of natural microbial consortia using cultivationindependent methods [3][4][5] . Metagenomic analyses have provided a new dimension in the study of community organization and metabolism in natural microbial communities [6][7][8][9][10] .To date, however, genomic analyses of symbiotic microbes from eukaryotes have been confined to individual strains (for the only exception see Wu et al. 11), limiting our ability to understand the intricate interactions involving communication, competition, and resource partitioning that shape symbiotic microbial communities.Here, we used random shotgun sequencing and nucleotide-signature based binning to study the symbiotic community in Olavius algarvensis. This marine worm belongs to a group of oligochaetes (phylum Annelida) that lack a mouth, gut, and anus, and are unique among annelid worms in having reduced their nephridial excretory system 12 . They live in obligate and species-specific associations with multiple extracellular bacterial endosymbionts located just below the worm cuticle 12 . Since the symbionts have yet to be grown in culture, their phylogeny has only been accessible through 16S rRNA analysis and fluorescence in situ hybridization (FISH) 13,14 . O. algarvensis lives in coastalMediterranean sediments and harbors a chemoautotrophic sulfur-oxidizing Gammaproteobacterium ( 1 symbiont) and a deltaproteobacterial sulfate reducer ( 1 symbiont), recently shown to be engaged in an endosymbiotic sulfur cycle 14. An additional gamma-and deltaproteobacterial symbiont ( 3 and 4 symbionts) of ...
Pirellula sp. strain 1 (''Rhodopirellula baltica'') is a marine representative of the globally distributed and environmentally important bacterial order Planctomycetales. Here we report the complete genome sequence of a member of this independent phylum. With 7.145 megabases, Pirellula sp. strain 1 has the largest circular bacterial genome sequenced so far. The presence of all genes required for heterolactic acid fermentation, key genes for the interconversion of C1 compounds, and 110 sulfatases were unexpected for this aerobic heterotrophic isolate. Although Pirellula sp. strain 1 has a proteinaceous cell wall, remnants of genes for peptidoglycan synthesis were found. Genes for lipid A biosynthesis and homologues to the flagellar L-and P-ring protein indicate a former Gram-negative type of cell wall. Phylogenetic analysis of all relevant markers clearly affiliates the Planctomycetales to the domain Bacteria as a distinct phylum, but a deepest branching is not supported by our analyses. P irellula sp. strain 1, which is in the process of being validly described as ''Rhodopirellula baltica,'' is a marine, aerobic, heterotrophic representative of the globally distributed and environmentally important bacterial order Planctomycetales. Molecular microbial ecology studies repeatedly provided evidence that planctomycetes are abundant in terrestrial and marine habitats (1-5). For example, they inhabit phytodetrital macroaggregates in marine environments (6) and include one of the organisms known to derive energy from the anaerobic oxidation of ammonia (7). They catalyze important transformations in global carbon and nitrogen cycles. By their mineralization of marine snow particles planctomycetes have a profound impact on global biogeochemistry and climate by affecting exchange processes between the geosphere and atmosphere (8). From a phylogenetic perspective the order Planctomycetales forms an independent, monophyletic phylum of the domain Bacteria (9). It has recently been suggested to be the deepest branching bacterial phylum (10). Planctomycetes are unique in many other respects. Their cell walls do not contain peptidoglycan, the main structural polymer of most members of the domain Bacteria. They show a unique cell compartmentalization in which a single membrane separates a peripheral ribosome-free paryphoplasm from the inner riboplasm (pirellulosome). Within the riboplasm, all planctomycetes contain a condensed fibrillar nucleoid, which in Gemmata spp. is surrounded by a additional double membrane (11). These structures, together with an unusual fatty acid composition of the phospholipids, resemble eukaryotes rather than a representative of the bacterial domain (12).Characteristic for Planctomycetales are the polar cell organization and a life cycle with a polar, yeast-like cell division. Cells attach to surfaces at their vegetative poles by means of an excreted holdfast substance or stalks (13). Further unusual features are the crateriform structures on the cell surface of all planctomycetes (14). They appear as...
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