Search bioRxiv⌕ Search

Biology subjects

Arnosti, C.

Publications and source records attributed to Arnosti, C..

9 recordsLinked to original sources

Macroalgal fucoidan can activate the biological carbon pump

Macroalgae secrete complex carbohydrate polymers, their extracellular matrix, as protection against microbial degradation. By resisting breakdown, these carbohydrates can contribute to marine carbon sequestration, though mechanisms, extent, and timescales remain unknown. Using ship-based sampling and experiments, we found that brown macroalgae release 1.7-4.2% of carbon fixation as fucoidan, equivalent to 0.32-0.88 mg fucoidan per gram of dry seaweed tissue per day. A Bayesian model trained on our empirical data, coupled with Monte Carlo simulations suggests an annual global release of 13-37 megatons fucoidan carbon. Moreover, degradation resistance combined with surface-activity enabled fucoidan to act as glue that cross-linked allochthonous organic carbon including microbes and proteins into marine snow. Notably, substantial fucoidan exudation was universally conserved across all tested species and regions. Thus, any brown macroalgal species can be used e.g. via aquafarming to enhance the formation of marine snow.

ecology↗

Effects of increasing hydrostatic pressures on marine microbial enzymatic activities

High hydrostatic pressure is characteristic of the deep ocean and presumed to influence microbial functions and viability. However, marine microbial processes are typically measured only at atmospheric pressure (0.1 MPa), limiting our understanding of pressure effects on the activities of microbes that sink as part of the biological carbon pump as well as those that reside in the deep ocean. To test pressure effects on microbial functions, we measured extracellular enzymatic activities--the first step in organic matter remineralization--of a moderate piezophile (Photobacterium profundum SS9), as well as of microbial communities in waters and sediments from shallow to abyssal (5,500 m) depths and their cell-free enzymes (<0.2 {micro}m). Activities were measured at 0.1-100 MPa to assess the pressure effects across the nearly full range of oceanic depths. P. profundum SS9 enzymes show varying pressure effects, from considerable stimulation at optimal pressure (28 MPa) to near complete inhibition (100 MPa). Pressure effects were measured for diverse protein- and carbohydrate-degrading and phosphorus-acquiring enzymes among pelagic and benthic microbial communities. The most common pressure effect is partial activity reduction, indicating a dampening of the initial step of carbon remineralization at increasing pressures. However, retention of cell-free enzymatic activities at higher pressures was occasionally observed even for enzymes from surface-originating assemblages, indicating functionality down to hadal depths and their potential for piezotolerance. These variable pressure effects must be considered when quantifying degradation rates of sinking and deposited particulate matter at increasing pressures in the deep ocean.

ecology↗

Selective preservation of fucose-rich oligosaccharides in the North Atlantic Ocean

The ocean has a substantial capacity to store carbon dioxide fixed via photosynthesis in dissolved organic molecules. An estimated 20% of the 660 Gt dissolved organic carbon in the ocean pool consists of structurally uncharacterized oligosaccharides, which appear to resist microbial degradation (Aluwihare et al., 1997). Current technologies lack the sensitivity and molecular resolution to identify these oligosaccharides. Here, we adapted graphitized carbon chromatography to extract and separate marine oligosaccharides for liquid chromatography high resolution mass spectrometry analysis. Using a newly-developed de novo annotation tool, we found 110 oligosaccharide structures in surface and deep ocean seawater at two distant locations in the North Atlantic Ocean. One group of the detected oligosaccharides was found only in surface seawater and consisted of larger and more abundant molecules detected by our analysis. A second group of smaller, less abundant oligosaccharides was detected in both the surface and deep ocean seawater of both sampled locations. The composition of oligosaccharides differed between the surface and deep ocean, with deep ocean samples relatively enriched in hard-to-metabolize deoxy-sugars, and xylose, amino sugars and uronic acids compared to simple hexoses. Notably the deoxy-sugar fucose constituted 35-40% of the monomers in deep-sea oligosaccharides, twice the percentage in surface ocean oligosaccharides. The ubiquity of deep ocean oligosaccharides indicates that they represent a preserved fraction of the carbohydrate pool. Their enrichment in specific monosaccharides suggests selective preservation of fucose-rich oligosaccharides in the deep ocean.

ecology↗

Visualizing and identifying selfish bacteria: a hunting guide

Polysaccharides are dominant components of plant biomass, whose degradation is typically mediated by heterotrophic bacteria. These bacteria use extracellular enzymes to hydrolyze polysaccharides to oligosaccharides that are then also available to other bacteria. Recently, a new mechanism of polysaccharide processing - selfish uptake - has been recognized, initially among gut-derived bacteria. In selfish uptake, polysaccharides are bound at the outer membrane, partially hydrolyzed, and transported into the periplasmic space without loss of hydrolysis products, thus limiting the availability of smaller sugars to the surrounding environment. Selfish uptake is widespread in environments ranging from the oceans cool, oxygen-rich, organic carbon-poor waters to the warm, carbon-rich, anoxic environment of the human gut. We provide a detailed guide of how to hunt for selfish bacteria, including how to rapidly visualize selfish uptake in complex bacterial communities, identify selfish organisms, and distinguish the activity of selfish organisms from other members of the community.

microbiology↗

Selfish bacteria are active throughout the water column of the ocean

Heterotrophic bacteria use extracellular enzymes to hydrolyze high molecular weight (HMW) organic matter to low molecular weight (LMW) hydrolysis products that can be taken into the cell. These enzymes represent a considerable investment of carbon, nitrogen, and energy, yet the return on this investment is uncertain, since hydrolysis of a HMW substrate outside a cell yields LMW products that can be lost to diffusion and taken up by scavengers that do not produce extracellular enzymes1. However, an additional strategy of HMW organic matter utilization, selfish uptake2, is used for polysaccharide degradation, and has recently been found to be widespread among bacterial communities in surface ocean waters3. During selfish uptake, polysaccharides are bound at the cell surface, initially hydrolyzed, and transported into the periplasmic space without loss of hydrolysis products2, thereby retaining hydrolysate for the selfish bacteria and reducing availability of LMW substrates to scavenging bacteria. Here we show that selfish bacteria are common not only in the sunlit upper ocean, where polysaccharides are freshly produced by phytoplankton, but also deeper in the oceanic water column, including in bottom waters at depths of more than 5,500 meters. Thus, the return on investment, and therefore also the supply of suitable polysaccharides, must be sufficient to maintain these organisms.

microbiology↗

A Sea Change in Microbial Enzymes: Heterogeneous latitudinal and depth-related gradients in bulk water and particle-associated enzymatic activities from 30°S to 59°N in the Pacific Ocean

Heterotrophic microbes initiate organic matter degradation using extracellular enzymes. Our understanding of differences in microbial enzymatic capabilities, especially among particle-associated taxa and in the deep ocean, is limited by a paucity of hydrolytic enzyme activity measurements. Here, we measured the activities of a broad range of hydrolytic enzymes (glucosidases, peptidases, polysaccharide hydrolases) in epipelagic to bathypelagic bulk water (non-size fractionated), and on particles ([&ge;] 3 m) along a 9,800 km latitudinal transect from 30{degrees}S in the South Pacific to 59{degrees}N in the Bering Sea. Individual enzyme activities showed heterogeneous latitudinal and depth-related patterns, with varying biotic and abiotic correlates. With increasing latitude and decreasing temperature, lower laminarinase activities sharply contrasted with higher leucine aminopeptidase (leu-AMP) and chondroitin sulfate hydrolase activities in bulk water. Endopeptidases (chymotrypsins, trypsins) exhibited patchy spatial patterns, and their activities can exceed rates of the widely-measured exopeptidase, leu-AMP. Compared to bulk water, particle-associated enzymatic profiles featured a greater relative importance of endopeptidases, a broader spectrum of polysaccharide hydrolases, and latitudinal and depth-related trends that paralleled variations in particle fluxes. As water depth increased, enzymatic spectra on particles and in bulk water became narrower, and diverged more from one another. These distinct latitudinal and depth-related gradients of enzymatic activities underscore the biogeochemical consequences of emerging global patterns of microbial community structure and function, from surface to deep waters, and among particle-associated taxa.

microbiology↗

Quantifying fluorescent glycan uptake to elucidate strain-level variability in foraging behaviors of rumen bacteria

Gut microbiomes have vast catabolic potential and are essential to host health and nutrition. An in-depth understanding of the metabolic pathways in these ecosystems will enable us to design treatments (i.e. prebiotics) that influence microbiome structure and enhance host physiology. Currently, the investigation of metabolic pathways relies on inferences derived from metagenomics or in vitro cultivations, however, novel approaches targeting specific cell physiologies can illuminate the functional potential encoded within microbial (meta)genomes to accurately assess metabolic abilities. Here, we present a multi-faceted study using complimentary next-generation physiology and omics approaches to characterize the microbial adaptation to a prebiotic in the rumen ecosystem. Using fluorescently labeled polysaccharides, we identified bacteria that actively metabolize a glycan prebiotic in the rumen microbiome ex vivo. Subsequently, we characterized strain-level variability in carbohydrate utilization systems and predict metabolic strategies of isolated bovine-adapted strains of Bacteroides thetaiotaomicron using comparative whole genome sequencing, RNA-Seq, and carbohydrate-active enzyme fingerprinting.

microbiology↗

Short-term changes in polysaccharide utilization mechanisms of marine bacterioplankton during a spring phytoplankton bloom

Spring phytoplankton blooms in temperate environments contribute disproportionately to global marine productivity. Bloom-derived organic matter, much of it occurring as polysaccharides, fuels biogeochemical cycles driven by interacting autotrophic and heterotrophic communities. We tracked changes in the mode of polysaccharide utilization by heterotrophic bacteria during the course of a diatom-dominated bloom in the German Bight, North Sea. Polysaccharides can be taken up in a selfish mode, where initial hydrolysis is coupled to transport into the periplasm, such that little to no low molecular weight (LMW) products are externally released to the environment. Alternatively, polysaccharides hydrolyzed by cell-surface attached or free extracellular enzymes (external hydrolysis) yield LMW products available to the wider bacterioplankton community. In the early bloom phase, selfish activity was accompanied by low extracellular hydrolysis rates of a few polysaccharides. As the bloom progressed, selfish uptake increased markedly, and external hydrolysis rates increased, but only for a limited range of substrates. The late bloom phase was characterized by high external hydrolysis rates of a broad range of polysaccharides, and reduced selfish uptake of polysaccharides, except for laminarin. Substrate utilization mode is related both to substrate structural complexity and to the bloom-stage dependent composition of the heterotrophic bacterial community. Originality statementThe means by which heterotrophic bacteria cooperate and compete to obtain substrates is a key factor determining the rate and location at which organic matter is cycled in the ocean. Much of this organic matter is high molecular weight (HMW), and must be enzymatically hydrolyzed to smaller pieces to be processed by bacterial communities. Some of these enzyme-producing bacteria are selfish, processing HMW organic matter without releasing low molecular weight (LMW) products to the environment. Other bacteria hydrolyze HMW substrates in a manner that releases LMW products to the wider bacterial community. How these mechanisms of substrate hydrolysis work against a changing background of organic matter supply is unclear. Here, we measured changing rates and mechanisms of substrate processing during the course of a natural phytoplankton bloom in the North Sea. Selfish bacteria generally dominate in the initial bloom stages, but a greater supply of increasingly complex substrates in later bloom stages leads to external hydrolysis of a wider range of substrates, increasing the supply of LMW hydrolysis products to the wider bacterial community.

microbiology↗

Global ecotypes in the ubiquitous marine clade SAR86

SAR86 is an abundant and ubiquitous heterotroph in the surface ocean that plays a central role in the function of marine ecosystems. We hypothesized that despite its ubiquity, different SAR86 subgroups may be endemic to specific ocean regions and functionally specialized for unique marine environments. However, the global biogeographical distributions of SAR86 genes, and the manner in which these distributions correlate with marine environments, have not been investigated. We quantified SAR86 gene content across globally-distributed metagenomic samples and modeled these gene distributions as a function of 51 environmental variables. We identified five distinct clusters of genes within the SAR86 pangenome, each with a unique geographic distribution associated with specific environmental characteristics. Gene clusters are characterized by strong taxonomic enrichment of distinct SAR86 genomes and partial assemblies, as well as differential enrichment of certain functional groups, suggesting differing functional and ecological roles of SAR86 ecotypes. We then leveraged our models and high-resolution, remote sensing-derived environmental data to predict the distributions of SAR86 gene clusters across the worlds oceans, creating global maps of SAR86 ecotype distributions. Our results reveal that SAR86 exhibits previously unknown, complex biogeography, and provide a framework for exploring geographic distributions of genetic diversity from other microbial clades.

ecology↗