scholarly journals Carbon assimilating fungi from surface ocean to subseafloor revealed by coupled phylogenetic and stable isotope analysis

2021 ◽  
Author(s):  
William D. Orsi ◽  
Aurèle Vuillemin ◽  
Ömer K. Coskun ◽  
Paula Rodriguez ◽  
Yanik Oertel ◽  
...  

AbstractFungi are ubiquitous in the ocean and hypothesized to be important members of marine ecosystems, but their roles in the marine carbon cycle are poorly understood. Here, we use 13C DNA stable isotope probing coupled with phylogenetic analyses to investigate carbon assimilation within diverse communities of planktonic and benthic fungi in the Benguela Upwelling System (Namibia). Across the redox stratified water column and in the underlying sediments, assimilation of 13C-labeled carbon from diatom extracellular polymeric substances (13C-dEPS) by fungi correlated with the expression of fungal genes encoding carbohydrate-active enzymes. Phylogenetic analysis of genes from 13C-labeled metagenomes revealed saprotrophic lineages related to the facultative yeast Malassezia were the main fungal foragers of pelagic dEPS. In contrast, fungi living in the underlying sulfidic sediments assimilated more 13C-labeled carbon from chemosynthetic bacteria compared to dEPS. This coincided with a unique seafloor fungal community and dissolved organic matter composition compared to the water column, and a 100-fold increased fungal abundance within the subseafloor sulfide-nitrate transition zone. The subseafloor fungi feeding on 13C-labeled chemolithoautotrophs under anoxic conditions were affiliated with Chytridiomycota and Mucoromycota that encode cellulolytic and proteolytic enzymes, revealing polysaccharide and protein-degrading fungi that can anaerobically decompose chemosynthetic necromass. These subseafloor fungi, therefore, appear to be specialized in organic matter that is produced in the sediments. Our findings reveal that the phylogenetic diversity of fungi across redox stratified marine ecosystems translates into functionally relevant mechanisms helping to structure carbon flow from primary producers in marine microbiomes from the surface ocean to the subseafloor.

2009 ◽  
Vol 60 (1) ◽  
pp. 59-70 ◽  
Author(s):  
Patrícia Kováčová ◽  
Natália Hudáčková

Late Badenian foraminifers from the Vienna Basin (Central Paratethys): stable isotope study and paleoecological implicationsPaleoecological interpretations based on stable isotope study of benthic (Uvigerina semiornata) and planktonic (Globigerina bulloides, Globigerinoides trilobus) foraminiferal shells from the Paratethys Vienna Basin (southwestern Slovakia) are presented. The study was performed on sediments of the Devínska Nová Ves-clay pit deposited during the Middle and Late Badenian (Middle Miocene). Our δ13C data show an enhanced nutrient input to the water column and the organic matter accumulation at the bottom of the Vienna Basin. The remineralization of accumulated organic matter on the sea floor resulted in the formation of oxygen-depleted zones, where no oxic indicators but the oxygen-deficiency tolerant species were found. Positive benthic δ18O signal can be attributed to the influence of the global cooling recognized in the world-ocean during the Middle Miocene. At the same time, variations observed in the water column are interpreted as reflecting the local temperature and salinity changes resulting from the fluvial and rain inflow. The differences between surface and bottom water temperature reflect the stratification of the water column. Such stratification might be related to the isolation process of Central Paratethys in the Badenian. This study confirms that δ13C and δ18O are not always in isotopic equilibrium with the ambient water but are also influenced by vital effects (respiration, symbiont photosynthesis …). The vital effects led to the incorporation of isotopically light metabolic CO2intoGlobigerina bulloidesresulting in high similarity between δ13C values ofUvigerinaandGlobigerina. It has been shown that the extremely high δ13C and very low δ18O ofGlobigerinoides trilobusclearly imply the influence of algal photosymbionts.


2020 ◽  
Vol 11 ◽  
Author(s):  
Shuting Liu ◽  
Nicholas Baetge ◽  
Jacqueline Comstock ◽  
Keri Opalk ◽  
Rachel Parsons ◽  
...  

2021 ◽  
Author(s):  
Greta Giljan ◽  
Sarah Brown ◽  
C. Chad Lloyd ◽  
Sherif Ghobrial ◽  
Rudolf Amann ◽  
...  

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.


2006 ◽  
Vol 73 (4) ◽  
pp. 1041-1048 ◽  
Author(s):  
G. Lear ◽  
B. Song ◽  
A. G. Gault ◽  
D. A. Polya ◽  
J. R. Lloyd

ABSTRACT The health of millions is threatened by the use of groundwater contaminated with sediment-derived arsenic for drinking water and irrigation purposes in Southeast Asia. The microbial reduction of sorbed As(V) to the potentially more mobile As(III) has been implicated in release of arsenic into groundwater, but to date there have been few studies of the microorganisms that can mediate this transformation in aquifers. With the use of stable isotope probing of nucleic acids, we present evidence that the introduction of a proxy for organic matter (13C-labeled acetate) stimulated As(V) reduction in sediments collected from a Cambodian aquifer that hosts arsenic-rich groundwater. This was accompanied by an increase in the proportion of prokaryotes closely related to the dissimilatory As(V)-reducing bacteria Sulfurospirillum strain NP-4 and Desulfotomaculum auripigmentum. As(V) respiratory reductase genes (arrA) closely associated with those found in Sulfurospirillum barnesii and Geobacter uraniumreducens were also detected in active bacterial communities utilizing 13C-labeled acetate in microcosms. This study suggests a direct link between inputs of organic matter and the increased prevalence and activity of organisms which transform As(V) to the potentially more mobile and thus hazardous As(III) via dissimilatory As(V) reduction.


2020 ◽  
Vol 86 (7) ◽  
Author(s):  
Yali Kong ◽  
Yakov Kuzyakov ◽  
Yang Ruan ◽  
Junwei Zhang ◽  
Tingting Wang ◽  
...  

ABSTRACT Decomposition of crop residues in soil is mediated by microorganisms whose activities vary with fertilization. The complexity of active microorganisms and their interactions utilizing residues is impossible to disentangle without isotope applications. Thus, 13C-labeled rice residues were employed, and DNA stable-isotope probing (DNA-SIP) combined with high-throughput sequencing was applied to identify microbes active in assimilating residue carbon (C). Manure addition strongly modified microbial community compositions involved in the C flow from rice residues. Relative abundances of the bacterial genus Lysobacter and fungal genus Syncephalis were increased, but abundances of the bacterial genus Streptomyces and fungal genus Trichoderma were decreased in soils receiving mineral fertilizers plus manure (NPKM) compared to levels in soils receiving only mineral fertilizers (NPK). Microbes involved in the flow of residue C formed a more complex network in NPKM than in NPK soils because of the necessity to decompose more diverse organic compounds. The fungal species (Jugulospora rotula and Emericellopsis terricola in NPK and NPKM soils, respectively) were identified as keystone species in the network and may significantly contribute to residue C decomposition. Most of the fungal genera in NPKM soils, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded faster to residue addition than those in NPK soils. This is connected with the changes in the composition of the rice residue during degradation and with fungal adaptation (abundance and activity) to continuous manure input. Our findings provide fundamental information about the roles of key microbial groups in residue decomposition and offer important cues on manipulating the soil microbiome for residue utilization and C sequestration in soil. IMPORTANCE Identifying and understanding the active microbial communities and interactions involved in plant residue utilization are key questions to elucidate the transformation of soil organic matter (SOM) in agricultural ecosystems. Microbial community composition responds strongly to management, but little is known about specific microbial groups involved in plant residue utilization and, consequently, microbial functions under different methods of fertilization. We combined DNA stable-isotope (13C) probing and high-throughput sequencing to identify active fungal and bacterial groups degrading residues in soils after 3 years of mineral fertilization with and without manure. Manuring changed the active microbial composition and complexified microbial interactions involved in residue C flow. Most fungal genera, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded to residue addition faster in soils that historically had received manure. We generated a valuable library of microorganisms involved in plant residue utilization for future targeted research to exploit specific functions of microbial groups in organic matter utilization and C sequestration.


2018 ◽  
Vol 84 (18) ◽  
Author(s):  
Ömer K. Coskun ◽  
Monica Pichler ◽  
Sergio Vargas ◽  
Stuart Gilder ◽  
William D. Orsi

ABSTRACTBenthic environments harbor highly diverse and complex microbial communities that control carbon fluxes, but the role of specific uncultivated microbial groups in organic matter turnover is poorly understood. In this study, quantitative DNA stable isotope probing (DNA-qSIP) was used for the first time to link uncultivated populations of bacteria and archaea to carbon turnover in lacustrine surface sediments. After 1-week incubations in the dark with [13C]bicarbonate, DNA-qSIP showed that ammonia-oxidizing archaea (AOA) were the dominant active chemolithoautotrophs involved in the production of new organic matter. Natural13C-labeled organic matter was then obtained by incubating sediments in the dark for 2.5 months with [13C]bicarbonate, followed by extraction and concentration of high-molecular-weight (HMW) (>50-kDa) organic matter. qSIP showed that the labeled organic matter was turned over within 1 week by 823 microbial populations (operational taxonomic units [OTUs]) affiliated primarily with heterotrophicProteobacteria,Chloroflexi,Verrucomicrobia, andBacteroidetes. However, several OTUs affiliated with the candidate microbial taxaLatescibacteria,Omnitrophica,Aminicentantes,Cloacimonates,AC1,Bathyarchaeota, andWoesearchaeota, groups known only from genomic signatures, also contributed to biomass turnover. Of these 823 labeled OTUs, 52% (primarily affiliated withProteobacteria) also became labeled in 1-week incubations with [13C]bicarbonate, indicating that they turned over carbon faster than OTUs that were labeled only in incubations with13C-labeled HMW organic matter. These taxa consisted primarily of uncultivated populations within theFirmicutes,Bacteroidetes,Verrucomicrobia, andChloroflexi, highlighting their ecological importance. Our study helps define the role of several poorly understood, uncultivated microbial groups in the turnover of benthic carbon derived from “dark” primary production.IMPORTANCELittle is known about the ecological role of uncultivated microbial populations in carbon turnover in benthic environments. To better understand this, we used quantitative stable isotope probing (qSIP) to quantify the abundance of diverse, specific groups of uncultivated bacteria and archaea involved in autotrophy and heterotrophy in a benthic lacustrine habitat. Our results provide quantitative evidence for active heterotrophic and autotrophic metabolism of several poorly understood microbial groups, thus demonstrating their relevance for carbon turnover in benthic settings. Archaeal ammonia oxidizers were significant drivers ofin situ“dark” primary production supporting the growth of heterotrophic bacteria. These findings expand our understanding of the microbial populations within benthic food webs and the role of uncultivated microbes in benthic carbon turnover.


2018 ◽  
Vol 20 (2) ◽  
pp. 815-827 ◽  
Author(s):  
William D. Orsi ◽  
Susanne Wilken ◽  
Javier del Campo ◽  
Thierry Heger ◽  
Erick James ◽  
...  

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