Linking Uncultivated Microbial Populations and Benthic Carbon Turnover by Using Quantitative Stable Isotope Probing

Coskun, Oemer K.; Pichler, Matthias; Vargas, Sergio; Gilder, Stuart; Orsi, William D.

doi:10.1128/aem.01083-18

Cited by 42 publications

(56 citation statements)

References 70 publications

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“…Bacterial 16S rRNA gene V4 hypervariable region was performed with primer pair 515F/806R (Walters et al ., ) using the qPCR protocol described previously (Coskun et al ., ). In brief, qPCR was carried out in 20 μl solutions containing 10.4 μl SsoAdvanced SYBR green PCR buffer (Bio‐Rad, Hercules, CA, USA), 0.4 μl of 10 mM primer, 6.8 μl of nuclease‐free water and 2 μl of the DNA template.…”

Section: Methodsmentioning

confidence: 97%

Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon

Ortega‐Arbulú

Pichler

Vuillemin

et al. 2018

Environmental Microbiology

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Summary Fungi living in sediments (‘mycobenthos’) are hypothesized to play a role in the degradation of organic matter deposited at the land‐sea interface, but the environmental factors influencing the mycobenthos are poorly understood. We used mock community calibrated Illumina sequencing to show that the mycobenthos community structure in a coastal lagoon was significantly changed after exposure to a lignocellulose extract and subsequent development of benthic anoxia over a relatively short (10 h) incubation. Saprotrophic taxa dominated and were selected for under benthic anoxia, specifically Aquamyces (Chytridiomycota) and Orbilia (Ascomycota), implicating these genera as important benthic saprotrophs. Protein encoding genes involved in energy and biomass production from Fungi and the fungal‐analogue group Labyrinthulomycetes had the highest increase in expression with the added organic matter compared with all other groups, indicating that lignocellulose stimulates metabolic activity in the mycobenthos. Flavobacteria dominated the active bacterial community that grew rapidly with the lignocellulose extract and crashed sharply upon O2 depletion. Our findings indicate that the diversity, activity and trophic potential of the mycobenthos changes rapidly in response to organic matter and decreasing O2 concentrations, which together with heterotrophic Flavobacteria, undergo ‘boom and bust’ dynamics during lignocellulose degradation in estuarine ecosystems.

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Section: Methodsmentioning

confidence: 97%

Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon

Ortega‐Arbulú

Pichler

Vuillemin

et al. 2018

Environmental Microbiology

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“…The authors distinguished a fast initial consumption, which was attributed to low‐molecular compounds leaking from the diatoms, followed by a slower process, which was attributed to the decomposition of the more complex and high‐molecular EPS, which first had to be degraded by extracellular enzymes to low‐molecular compounds. A similar carbon transfer was found in a freshwater chemoautotrophic benthic community, although, in this case the consumers were more diverse and seemed to have a higher specialization (Coskun et al ., ). These differences may be attributed to the method, which was fundamentally different from the one used by Miyatake and colleagues ().…”

Section: The Role and Fate Of Eps In Benthic Phototrophic Communitiesmentioning

confidence: 97%

“…Bacteroidetes and Actinobacteria were the other two abundant groups and showed less notable differences along the tidal gradient. These two groups are important as chemoheterotrophic organisms, specialized in the degradation of complex organic matter and play, therefore, a crucial role in the carbon cycle in the mats (Coskun et al, 2018). Sulfate-reducing bacteria and (phototrophic) sulfur-oxidizing bacteria belong roughly to the Deltaproteobacteria and Gammaproteobacteria, respectively, and this explains their higher abundance in the marine and brackish mats.…”

Section: Diversity Of Microbial Mats and Diatom Biofilmsmentioning

confidence: 99%

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

Stal

Bolhuis

Cretoiu

2018

Environmental Microbiology

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Summary Phototrophic biofilms are multispecies, self‐sustaining and largely closed microbial ecosystems. They form macroscopic structures such as microbial mats and stromatolites. These sunlight‐driven consortia consist of a number of functional groups of microorganisms that recycle the elements internally. Particularly, the sulfur cycle is discussed in more detail as this is fundamental to marine benthic microbial communities and because recently exciting new insights have been obtained. The cycling of elements demands a tight tuning of the various metabolic processes and require cooperation between the different groups of microorganisms. This is likely achieved through cell‐to‐cell communication and a biological clock. Biofilms may be considered as a macroscopic biological entity with its own physiology. We review the various components of some marine phototrophic biofilms and discuss their roles in the system. The importance of extracellular polymeric substances (EPS) as the matrix for biofilm metabolism and as substrate for biofilm microorganisms is discussed. We particularly assess the importance of extracellular DNA, horizontal gene transfer and viruses for the generation of genetic diversity and innovation, and for rendering resilience to external forcing to these biological entities.

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“…After 10 days the flasks were frozen until processing for SIP. DNA from the samples was extracted as described above and prepared for density gradient centrifugation according to the quantitative stable isotope probing protocol as described previously 45 . In brief, density gradient centrifugations were carried out in a TLN-100 Optima MAX-TL ultracentrifuge (Beckman Coulter, Brea, CA, USA) near-vertical rotor at 18 °C for 72 h at 165,000 × g. 50 µL of DNA spanning from 0.5 µg to 1.5 µg which was within the range of proposed values 57 was added to a solution of cesium chloride (CsCl) and gradient buffer (0.1 M Tris, 0.1 M KCl and 1 mM EDTA) in order to achieve a starting density of 1.70 g mL -1 in a 3.3 mL polyallomer OptiSeal tubes (Beckman Coulter, Brea, CA, USA).…”

Section: Normalizing Gene Expressionmentioning

confidence: 99%

“…DNA was quantified fluorometrically using a Qubit. The observed excess atom 13 Cenrichment fraction (EAF) was calculated for each taxon according to a previously described study 45 using a qSIP workflow embedded in the HTS-SIP R package 58 . Weighted average densities were calculated for each taxon's DNA in the control ( 12 C added) and in the experimental incubation ( 13 C added) as described Hungate et al 59 to estimate the atom fraction excess of 13 C for each OTU.…”

Section: Normalizing Gene Expressionmentioning

confidence: 99%

Lokiarchaeon exhibits homoacetogenesis

Vuillemin

Rodríguez

et al. 2019

Preprint

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The proposed Asgard superphylum of Archaea comprises the closest archaeal 19 relatives of eukaryotes, whose genomes hold clues pertaining to the nature host cell that 20 acquired the mitochondrion at the origin of eukaryotes 1-4 . Genomes of the Asgard candidate 21 Phylum 'Candidatus Lokiarchaeota' [Lokiarchaeon] suggest an acetogenic H2 -dependent 22 lifestyle 5 and mixotrophic capabilities 6 . However, data on the activity of Lokiarchaeon are 23 currently lacking, and the ecology of the host cell that acquired the mitochondrion is 24 debated 4,7 . Here, we show that in anoxic marine sediments underlying highly productive 25 waters on the Namibian continental shelf Lokiarchaeon gene expression increases with depth 26 below the seafloor, and was significantly different across a redox gradient spanning hypoxic 27 to sulfidic conditions. Notably, Lokiarchaeon increased expression of genes involved in 28 growth, carbohydrate metabolism, and the H2-dependent Wood-Ljungdahl (WLP) carbon 29 fixation pathway under the most reducing (sulfidic) conditions. Quantitative stable isotope 30 probing experiments revealed multiple populations of Lokiarchaeota utilizing both CO2 and 31 diatomaceous extracellular polymeric substances (dEPS) as carbon sources over a 10-day 32 incubation under anoxic conditions. This apparent anaerobic mixotrophic metabolism was 33 consistent with the expression of Lokiarchaeon genes involved in transport and fermentation 34 of sugars and amino acids. Remarkably, several Asgard populations were more enriched 35 with 13 C-dEPS compared to the community average, indicating a preference for dEPS as a 36 growth substrate. The qSIP and gene expression data indicate a metabolism of "Candidatus 37 Lokiarchaeota" similar to that of sugar fermenting homoacetogenic bacteria 8 , namely that 38 Lokiarchaeon can couple fermentative H2 production from organic substrates with electron 39 bifurcation and the autotrophic and H2-dependent WLP. Homoacetogenesis allows to access 40 a wide range of substrates and relatively high ATP gain during acetogenic sugar 41 fermentation 8 thereby providing an ecological advantage for Lokiarchaeon in anoxic, energy 42 limited settings. 43 The Benguela upwelling system is one of the most productive ecosystems of the world's 44 oceans and exhibits an oxygen minimum zone (OMZ) overlying the seafloor on the Namibian 45 continental shelf 9 . Below the Namibian seafloor relatively high amounts of sulfide (H2S) and H2 46 are produced by sulfate reduction and microbial fermentation, respectively 10 . During the Southern 47

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Linking Uncultivated Microbial Populations and Benthic Carbon Turnover by Using Quantitative Stable Isotope Probing

Cited by 42 publications

References 70 publications

Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon

Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

Lokiarchaeon exhibits homoacetogenesis

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