ArticlePublisher preview available

Acetoclastic archaea adaptation under increasing temperature in lake sediments and wetland soils from Alaska

March 2023
Polar Biology 46(4):1-17

DOI:10.1007/s00300-023-03120-0

Authors:

Bruna Martins Dellagnezze

Northumbria University

Patricia Bovio Winkler

Clemente Estable Biological Research Institute

Céline Lavergne

Spanish National Research Council

Show all 8 authorsHide

The activity of methanogenic archaea is expected to be strongly affected under warmer temperatures, with higher greenhouse gas (GHG) emissions in the Arctic. In the sub-Arctic and Arctic freshwater sediments and wetland soils, acetoclastic methanogenesis is one of the major processes involved in methane (CH4) release. To investigate the microbial adaptation/ tolerance at warmer temperatures and high acetate concentration, anaerobic microcosms of lake sediments and wetland soils from sub-Arctic ecosystems from Denali to Toolik regions in Alaska (USA) were set up at four temperatures (5, 10, 15 and 20 °C). In both environmental and microcosm samples, archaeal diversity was evaluated through specific archaeal 16S rRNA sequencing as well as bacterial, archaeal and methanogen abundance using quantitative PCR. Acetate amendment strongly modified the archaeal diversity highly favoring methanogens from Methanosarcinales, and in lower abundance, Methanoregula and Bathyarchaeia in some lake sediment. While acetoclastic groups significantly diverged among aquatic and terrestrial ecosystems, temperature did not significantly shape methanogens’ diversity, showing their adaptability under warmer conditions. Faster microbial response on CH4 production rates was observed at warmer temperatures (15 and 20 °C), bringing insights on the psychrophilic acetoclastic groups adapted to high acetate concentration with potential biotechnological application.

Sampling spots location of four lakes and two wetland in Alaska: Lake Killarney (L1) and adjacent wetland (W1), Otto (L2), Nutella (L3), Goldstream Lake (L4), and in the north, one wetland within Toolik Lake area (W2) Source: Google Earth

…

Boxplot representing the influence of temperature on both CH4 production rates (panel a) and latency periods (panel b) in acetate-amended microcosms from lakesediments and wetland soils. Type of freshwater systems was plotted by different shapes and the 6 ecosystems were represented by colors. For wetland soils, distinction was made between top (T) (disks) and bottom (B) (open circles) samples

…

Principal component analysis (PCA) performed with seven variables showing the correlation between CH4 production rates (MPRs measured at 5, 10, 15 and 20 °C) and in situ samples physicochemical data. Left panel a showed the correlation plot of variables and right panel b showed the site position on the ordination colored by ecosystem, while the symbol shape represents the different ecosystem types. Significant segregation by biome (PERMANOVA, F = 4.18, p-value < 0.05) was plotted as spiders (95% confidence level). OM stands for organic matter and NOx for nitrates + nitrites

…

Microbial composition according to archaeal 16S rRNA gene sequence analysis. Heat map showing the relative abundance at genus level in all samples: in situ and incubated at different temperatures 5, 10, 15 and 20 °C

…

a Heat map showing the ASVs relative abundance. In the heatmap a color code was used where the red means higher relative abundance and blue color means the lower relative abundance values; b Venn diagram showing the number of ASVs shared within the different samples including a comparison between in situ samples and samples taken after incubation at 5 and 20 °C. The samples were separated into sediment lake (L) and wetland (WS) samples

…

Figures - available from: Polar Biology

This content is subject to copyright. Terms and conditions apply.

A preview of this full-text is provided by Springer Nature.

Learn more

Content available from Polar Biology

This content is subject to copyright. Terms and conditions apply.

Vol.:(0123456789)

1 3

Polar Biology (2023) 46:259–275

https://doi.org/10.1007/s00300-023-03120-0

ORIGINAL PAPER

Acetoclastic archaea adaptation underincreasing temperature inlake

sediments andwetland soils fromAlaska

B.M.Dellagnezze1· P.Bovio‑Winkler1· C.Lavergne2,3· D.A.Menoni1· F.Mosquillo1· L.Cabrol4,5,3· M.Barret6·

C.Etchebehere1

Received: 3 June 2022 / Revised: 13 February 2023 / Accepted: 22 February 2023 / Published online: 14 March 2023

Abstract

The activity of methanogenic archaea is expected to be strongly aﬀected under warmer temperatures, with higher green-

house gas (GHG) emissions in the Arctic. In the sub-Arctic and Arctic freshwater sediments and wetland soils, acetoclastic

methanogenesis is one of the major processes involved in methane (CH4) release. To investigate the microbial adaptation/

tolerance at warmer temperatures and high acetate concentration, anaerobic microcosms of lake sediments and wetland

soils from sub-Arctic ecosystems from Denali to Toolik regions in Alaska (USA) were set up at four temperatures (5, 10, 15

and 20°C). In both environmental and microcosm samples, archaeal diversity was evaluated through speciﬁc archaeal 16S

rRNA sequencing as well as bacterial, archaeal and methanogen abundance using quantitative PCR. Acetate amendment

strongly modiﬁed the archaeal diversity highly favoring methanogens from Methanosarcinales, and in lower abundance,

Methanoregula and Bathyarchaeia in some lake sediment. While acetoclastic groups signiﬁcantly diverged among aquatic

and terrestrial ecosystems, temperature did not signiﬁcantly shape methanogens’ diversity, showing their adaptability under

warmer conditions. Faster microbial response on CH4 production rates was observed at warmer temperatures (15 and 20°C),

bringing insights on the psychrophilic acetoclastic groups adapted to high acetate concentration with potential biotechno-

logical application.

Keywords Methane· Acetoclastic· Archaeal community· 16S rRNA sequencing· qPCR

Introduction

The Arctic has been one of the most susceptible regions

to the eﬀects of climate change, altering its landscape and

aﬀecting microbial activity. Constant warming has been

changing several physicochemical parameters, interfering

on microbial response, resulting in larger carbon input in

atmosphere (Cavicchioli etal. 2019). These changes are

also mentioned for Alaska state, which since the 1925s has

warmed almost two times higher compared to the whole

United States (Brooke etal. 2022).

High latitude wetlands and freshwater ecosystems (lakes,

ponds) represent one of the largest sources of the green-

house gas methane (CH4), accounting for more than 40%

of natural CH4 emissions (Cui etal. 2015; Wik etal. 2016;

Rosentreter etal. 2021). In these ecosystems, biogenic CH4

is mainly derived from methanogenic archaea harboring the

methyl-coenzyme M reductase (mcr), involved in the last

step of methanogenesis process (Steinberg and Regan 2009;

He etal. 2015). Methane can be produced through diﬀerent

* C. Etchebehere

cetchebehere@iibce.edu.uy

1 Microbial Ecology Laboratory, Department ofMicrobial

Biochemistry andGenomic, Biological Research

Institute “Clemente Estable”, Av Italia 15 3318,

CP11600Montevideo, Uruguay

2 HUB AMBIENTAL UPLALaboratory ofAquatic

Environmental Research Centro de Estudios Avanzados,

Universidad de Playa Ancha, Valparaíso, Chile

3 Escuela Ingeniería Bioquímica, Pontiﬁcia Universidad

Católica de Valparaíso, 2085Valparaíso, AvenidaBrasil,

Chile

4 Aix-Marseille Université, Univ Toulon, CNRS, IRD–

Mediterranean Institute ofOceanography (MIO, UM 110),

Marseille, France

5 Millenium Institute BASE “Biodiversity ofAntarctic

andSubantarctic Ecosystems”, Santiago, Chile

6 Laboratoire ´Ecologie Fonctionnelle et Environnement,

Université de Toulouse, CNRS, Toulouse, France

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Microbial community evolution in a lab-scale reactor operated to obtain biomass for biochemical methane potential assays

Article

Full-text available

Nov 2024
APPL MICROBIOL BIOT

Biochemical methane potential (BMP) test is an important tool to evaluate the methane production biodegradability and toxicity of different wastes or wastewaters. This is a key parameter for assessing design and feasibility issues in the full-scale implementation of anaerobic digestion processes. A standardized and storable inoculum is the key to obtain reproducible results. In Uruguay, a local enterprise dedicated to design and install anaerobic digesters operated a lab-scale bioreactor as a source of biomass for BMP tests, using a protocol previously described. This reactor was controlled and fed with a mixture of varied organic compounds (lipids, cellulolytic wastes, proteins). Biomass was reintroduced into the reactor after BMP assays to maintain a constant volume and biomass concentration. The aim of this work was to evaluate how the microbial community evolved during this operation and the effect of storing biomass in the refrigerator. The composition of the microbial communities was analyzed by 16S rRNA amplicon sequencing using primers for Bacteria and Archaea. The methanogenic activity was determined, and the methanogens were quantified by mcrA qPCR. One sample was stored for a 5-month period in the refrigerator (4 °C); the activity and the microbial community composition were analyzed before and after storage. Results showed that applying the reported methodology, a reliable methanogenic sludge with an acceptable SMA was obtained even though the reactor suffered biomass alterations along the evaluated period. Refrigerating the acclimatized biomass for 5 months did not affect its activity nor its microbial composition according to the 16S rRNA gene sequence analysis, even though changes in the mcrA abundance were observed. Key points • The applied methodology was successful to obtain biomass suitable to perform BMP assays. • The microbial community was resilient to external biomass addition. • Biomass storage at 4 °C for 5 months did not alter the methanogenic activity. Graphical Abstract

Genome‐Enabled Parameterization Enhances Model Simulation of CH4 Cycling in Four Natural Wetlands

Article

Full-text available

Sep 2024

Microbial processes are crucial in producing and oxidizing biological methane (CH4) in natural wetlands. Therefore, modeling methanogenesis and methanotrophy is advantageous for accurately projecting CH4 cycling. Utilizing the CLM‐Microbe model, which explicitly represents the growth and death of methanogens and methanotrophs, we demonstrate that genome‐enabled model parameterization improves model performance in four natural wetlands. Compared to the default model parameterization against CH4 flux, genomic‐enabled model parameterization added another contain on microbial biomass, notably enhancing the precision of simulated CH4 flux. Specifically, the coefficient of determination (R²) increased from 0.45 to 0.74 for Sanjiang Plain, from 0.78 to 0.89 for Changbai Mountain, and from 0.35 to 0.54 for Sallie's Fen, respectively. A drop in R² was observed for the Dajiuhu nature wetland, primarily caused by scatter data points. Theil's coefficient (U) and model efficiency (ME) confirmed the model performance from default parameterization to genome‐enabled model parameterization. Compared with the model solely calibrated to surface CH4 flux, additional constraints of functional gene data led to better CH4 seasonality; meanwhile, genome‐enabled model parameterization established more robust associations between simulated CH4 production rates and environmental factors. Sensitivity analysis underscored the pivotal role of microbial physiology in governing CH4 flux. This genome‐enabled model parameterization offers a valuable promise to integrate fast‐cumulating genomic data with CH4 models to better understand microbial roles in CH4 in the era of climate change.

Biogeography of microbial communities in high-latitude ecosystems: Contrasting drivers for methanogens, methanotrophs and global prokaryotes

Article

Full-text available

Oct 2023
ENVIRON MICROBIOL

Methane-cycling is becoming more important in high-latitude ecosystems as global warming makes permafrost organic carbon increasingly available. We explored 387 samples from three high-latitudes regions (Siberia, Alaska and Patagonia) focusing on mineral/organic soils (wetlands, peatlands, forest), lake/pond sediment and water. Physicochemical, climatic and geographic variables were integrated with 16S rDNA amplicon sequences to determine the structure of the overall microbial communities and of specific methanogenic and methanotrophic guilds. Physicochemistry (especially pH) explained the largest proportion of variation in guild composition, confirming species sorting (i.e., environmental filtering) as a key mechanism in microbial assembly. Geographic distance impacted more strongly beta diversity for (i) methanogens and methanotrophs than the overall prokaryotes and, (ii) the sediment habitat, suggesting that dispersal limitation contributed to shape the communities of methane-cycling microorganisms. Bioindicator taxa characterising different ecological niches (i.e., specific combinations of geographic, climatic and physicochemical variables) were identified, highlighting the importance of Methanoregula as generalist methanogens. Methylocystis and Methylocapsa were key methanotrophs in low pH niches while Methylobacter and Methylomonadaceae in neutral environments. This work gives insight into the present and projected distribution of methane-cycling microbes at high latitudes under climate change predictions, which is crucial for constraining their impact on greenhouse gas budgets.

Temperature differently affected methanogenic pathways and microbial communities in sub-Antarctic freshwater ecosystems

Article

Full-text available

Apr 2021

Freshwater ecosystems are responsible for an important part of the methane (CH4) emissions which are likely to change with global warming. This study aims to evaluate temperature-induced (from 5 to 20 °C) changes on microbial community structure and methanogenic pathways in five sub-Antarctic lake sediments from Magallanes strait to Cape Horn, Chile. We combined in situ CH4 flux measurements, CH4 production rates (MPRs), gene abundance quantification and microbial community structure analysis (metabarcoding of the 16S rRNA gene). Under unamended conditions, a temperature increase of 5 °C doubled MPR while microbial community structure was not affected. Stimulation of methanogenesis by methanogenic precursors as acetate and H2/CO2, resulted in an increase of MPRs up to 127-fold and 19-fold, respectively, as well as an enrichment of mcrA-carriers strikingly stronger under acetate amendment. At low temperatures, H2/CO2-derived MPRs were considerably lower (down to 160-fold lower) than the acetate-derived MPRs, but the contribution of hydrogenotrophic methanogenesis increased with temperature. Temperature dependence of MPRs was significantly higher in incubations spiked with H2/CO2 (c. 1.9 eV) compared to incubations spiked with acetate or unamended (c. 0.8 eV). Temperature was not found to shape the total microbial community structure, that rather exhibited a site-specific variability among the studied lakes. However, the methanogenic archaeal community structure was driven by amended methanogenic precursors with a dominance of Methanobacterium in H2/CO2-based incubations and Methanosarcina in acetate-based incubations. We also suggested the importance of acetogenic H2-production outcompeting hydrogenotrohic methanogenesis especially at low temperatures, further supported by homoacetogen proportion in the microcosm communities. The combination of in situ-, and laboratory-based measurements and molecular approaches indicates that the hydrogenotrophic pathway may become more important with increasing temperatures than the acetoclastic pathway. In a continuously warming environment driven by climate change, such issues are crucial and may receive more attention.

Half of global methane emissions come from highly variable aquatic ecosystem sources

Article

Full-text available

Apr 2021
NAT GEOSCI

Atmospheric methane is a potent greenhouse gas that plays a major role in controlling the Earth’s climate. The causes of the renewed increase of methane concentration since 2007 are uncertain given the multiple sources and complex biogeochemistry. Here, we present a metadata analysis of methane fluxes from all major natural, impacted and human-made aquatic ecosystems. Our revised bottom-up global aquatic methane emissions combine diffusive, ebullitive and/or plant-mediated fluxes from 15 aquatic ecosystems. We emphasize the high variability of methane fluxes within and between aquatic ecosystems and a positively skewed distribution of empirical data, making global estimates sensitive to statistical assumptions and sampling design. We find aquatic ecosystems contribute (median) 41% or (mean) 53% of total global methane emissions from anthropogenic and natural sources. We show that methane emissions increase from natural to impacted aquatic ecosystems and from coastal to freshwater ecosystems. We argue that aquatic emissions will probably increase due to urbanization, eutrophication and positive climate feedbacks and suggest changes in land-use management as potential mitigation strategies to reduce aquatic methane emissions. Methane emissions from aquatic systems contribute approximately half of global methane emissions, according to meta-analysis of natural, impacted and human-made aquatic ecosystems and indicating potential mitigation strategies to reduce emissions.

Psychrophilic enzymes: structural adaptation, pharmaceutical and industrial applications

Article

Full-text available

Feb 2021
APPL MICROBIOL BIOT

Psychrophiles are cold-living microorganisms synthesizing enzymes that are permanently active at almost near-zero temperatures. Psychrozymes are supposed to be structurally more flexible than their homologous proteins. This structural flexibility enables these proteins to undergo conformational changes during catalysis and improve catalytic efficiency at low temperatures. The outstanding characteristics of the psychrophilic enzymes have attracted the attention of the scientific community to utilize them in a wide variety of industrial and pharmaceutical applications. In this review, we first highlight the current knowledge of the cold-adaptation mechanisms of the psychrophiles. In the sequel, we describe the potential applications of the enzymes in different biotechnological processes specifically, in the production of industrial and pharmaceutical products. Key points • Methods that organisms have evolved to survive and proliferate at cold environments. • The economic benefits due to their high activity at low and moderate temperatures. • Applications of the psychrophiles in biotechnological and pharmaceutical industry.

ampvis2: an R package to analyse and visualise 16S rRNA amplicon data

Preprint

Full-text available

Apr 2018

Microbial community analysis using 16S rRNA gene amplicon sequencing is the backbone of many microbial ecology studies. Several approaches and pipelines exist for processing the raw data generated through DNA sequencing and convert the data into OTU-tables. Here we present ampvis2, an R package designed for analysis of microbial community data in OTU-table format with focus on simplicity, reproducibility, and sample metadata integration, with a minimal set of intuitive commands. Unique features include flexible heatmaps and simplified ordination. By generating plots using the ggplot2 package, ampvis2 produces publication-ready figures that can be easily customised. Furthermore, ampvis2 includes features for interactive visualisation, which can be convenient for larger, more complex data. Availability ampvis2 is implemented in the R statistical language and is released under the GNU A-GPL license. Documentation website and source code is maintained at: https://github.com/MadsAlbertsen/ampvis2 Contact Mads Albertsen ( ma@bio.aau.dk )

Microbial Community Composition and Function in Sediments from the Pearl River Mouth Basin

Article

Full-text available

Aug 2020

This study was conducted to characterize the diversity and function of microbial communities in marine sediments of the Pearl River Mouth Basin (PRMB) in the South China Sea. The results showed that the bacterial and archaeal communities varied greatly with depth. Proteobacteria in bacterial communities and Nitrososphaeria and Woesearchaeota in archaeal communities were dominant in the shallow sediments (1–40 cm), while Chloroflexi in bacterial communities and Bathyarchaeia in archaeal communities were dominant in the deep sediments (50–200 cm). Regarding ecological functions based on the metatranscriptomic data, genes involved in various pathways of nitrogen metabolism and sulfur metabolism were observed in the tested sediment samples. Metagenomic analysis revealed that Proteobacteria contribute the most to nearly all genes involved in nitrogen and sulfur metabolism. Moreover, Thaumarchaeota contribute the most to certain genes involved in nitrification, denitrification and assimilatory sulfate reduction pathways. The most abundant bacterial genus, Candidatus Scalindua, is crucial for nitrification, dissimilatory nitrate reduction, denitrification and assimilatory sulfate reduction pathways.

Roles of Thermokarst Lakes in a Warming World

Article

Full-text available

Apr 2020
TRENDS MICROBIOL

Permafrost covers a quarter of the northern hemisphere land surface and contains twice the amount of carbon that is currently present in the atmosphere. Future climate change is expected to reduce its near-surface cover by over 90% by the end of the 21st century, leading to thermokarst lake formation. Thermokarst lakes are point sources of carbon dioxide and methane which release long-term carbon stocks into the atmosphere, thereby initiating a positive climate feedback potentially contributing up to a 0.39°C rise of surface air temperatures by 2300. This review describes the potential role of thermokarst lakes in a warming world and the microbial mechanisms that underlie their contributions to the global greenhouse gas budget.

The biotechnological potential of microbial communities from Antarctic soils and sediments: Application to low temperature biogenic methane production

Article

Apr 2022
J BIOTECHNOL

Anaerobic digestion (AD) is an attractive bioprocess for waste treatment and energy recovery through methane-rich biogas production. Under temperate to cold climate, the implementation of AD for low-organic load wastewater treatment has been limited to date, due to the energetic and economic cost of maintaining optimal mesophilic temperature. Hence, we aim at (i) exploring the biotechnological potential of a microbial inoculum from Antarctic soils and sediments to run AD at low temperatures; and (ii) evaluating the effect of temperature over a psychrophilic-mesophilic range on both methane production rates and microbial community composition. Methane production stimulated by acetate amendment was detected from 5 to 37 °C, with a maximum at 25 °C, corresponding to the highest relative abundance of methanogenic archaea (c. 21.4% of the total community). From 5 to 25 °C, the predominant methanogen was Methanosaeta, while it shifted to Methanocorpusculum at 30 °C. Compared with an industrial mesophilic sludge, the relative methane production rate at 5 °C (compared to the maximum) was 40% greater in the Antarctic inoculum. Microbial communities from permanently cold Antarctic sediments efficiently produce methane at low temperatures revealing a biotechnological potential for the treatment of low-organic load residues in cold regions.

Methanogenic archaea in peatlands

Article

Nov 2020
FEMS MICROBIOL LETT

Methane emission feedbacks in wetlands are predicted to influence global climate under climate change and other anthropogenic stressors. Herein, we review the taxonomy and physiological ecology of the microorganisms responsible for methane production in peatlands. Common in peat soils are five of the eight described orders of methanogens spanning three phyla (Euryarchaeota, Halobacterota and Thermoplasmatota). The phylogenetic affiliation of sequences found in peat suggest that members of the thus-far-uncultivated group Candidatus Bathyarchaeota (representing a fourth phylum) may be involved in methane cycling, either anaerobic oxidation of methane and/or methanogenesis, as at least a few organisms within this group contain the essential gene, mcrA, according to metagenomic data. Methanogens in peatlands are notoriously challenging to enrich and isolate; thus, much remains unknown about their physiology and how methanogen communities will respond to environmental changes. Consistent patterns of changes in methanogen communities have been reported across studies in permafrost peatland thaw where the resulting degraded feature is thermokarst. However much remains to be understood regarding methanogen community feedbacks to altered hydrology and warming in other contexts, enhanced atmospheric pollution (N, S and metals) loading and direct anthropogenic disturbances to peatlands like drainage, horticultural peat extraction, forestry and agriculture, as well as post-disturbance reclamation.

Methanogenesis in Soils, Wetlands, and Peat

Chapter

Jan 2019

Ecophysiology of Acetoclastic Methanogens

Chapter

Jul 2019

Acetate is the most important precursor for methane in the degradation of organic matter. Only two genera of methanogenic archaea, Methanosarcina and Methanothrix (former Methanosaeta), are able to grow with acetate as sole energy and carbon source. Phylogenetically, Methanosarcina and Methanothrix both belong to the Methanosarcinales. These two genera show besides morphological differences, interesting differences in physiology. Methanosarcina is a generalist that can grow on a variety of substrates, while Methanothrix specialized in growth on acetate. The acetate metabolism shows differences in acetate activation and energy conservation. At conditions that are less favorable for acetoclastic methanogens, syntrophic acetate oxidation may occur. This, however, is not further addressed here.

Acetoclastic archaea adaptation under increasing temperature in lake sediments and wetland soils from Alaska

Abstract and Figures

Recommended publications

Estimating Population Turnover Rates by Relative Quantification Methods Reveals Microbial Dynamics i...

Temperature increase affects acetate-derived methane production in Alaskan lake sediments and wetlan...

Temperature differently affected methanogenic pathways and microbial communities in sub-Antarctic fr...

Comparative Study of Methanogenic Pathways in the Sediments of Thermokarst and Polygenetic Yamal Lak...

The biotechnological potential of microbial communities from Antarctic soils and sediments: Applicat...