Anaerobes in Biogeochemical Cycles

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 24277

Special Issue Editors


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Guest Editor
Laboratory of Microbiology, Wageningen University & Research, Stippeneng 4, 6708 WE Wageningen, The Netherlands
Interests: bacteriology; microbiology; bacteria; anaerobic microbiology; microbial diversity; mcrobial physiology; water microbiology; syntrophy; microbial interactions

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Guest Editor
Laboratory of Microbiology, Wageningen University & Research, Stippeneng 4, 6708 WE Wageningen, The Netherlands
Interests: biodegradation; biofuels; biotechnology; environmental engineering; microbiology; anaerobic digestion; anaerobic microbiology; methane; fatty acids

Special Issue Information

Dear Colleagues,

Anaerobic microorganisms, Bacteria and Archaea, have an essential role in the global biogeochemical cycles. Anaerobes are redox specialists and are responsible for the natural recycling of redox-active chemical elements abundant in the biosphere (carbon, nitrogen, sulfur, iron, and phosphorus) as well as of various other elements present in small amounts, such as iron. Biogeochemical cycles influence our climate, wastewater treatment, biofuels production, are essential for food production, and contribute to important processes in our intestinal tract.
The anaerobic cycling of nutrients requires complex microbiome interactions. An exceptionally diverse world of microorganisms inhabits the anaerobic environments on earth. These microorganisms obtain their energy by fermentation and anaerobic respiration; in addition, phototrophic and chemoautotrophic processes operate in the absence of oxygen. Despite the fundamental importance of anaerobes, many uncertainties remain about them and the processes in which they are involved.
In this Special Issue of Microorganisms, dedicated to Anaerobes in Biogeochemical Cycles, we invite you to send your contributions concerning any aspects related to anaerobic microbes involved in biogeochemical and nutrient cycling or conversion, from the ecology of anaerobic habitats to the physiology of novel species, and from fundamental to applied aspects. 

Dr. Caroline M. Plugge
Dr. Diana Z. Sousa
Guest Editors

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Keywords

  • Anaerobic biogeochemical cycles
  • Anaerobic nutrient cycles
  • Anaerobic redox reactions
  • Anaerobic microorganisms
  • Omics of anaerobes
  • Microbial interactions
  • Carbon cycling
  • Sulfur cycling
  • Nitrogen cycling
  • Iron cycling
  • Thermodynamics

Published Papers (8 papers)

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Editorial

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2 pages, 161 KiB  
Editorial
Special Issue “Anaerobes in Biogeochemical Cycles”
by Caroline M. Plugge and Diana Z. Sousa
Microorganisms 2021, 9(1), 23; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9010023 - 23 Dec 2020
Viewed by 1376
Abstract
Anaerobic microorganisms, Bacteria and Archaea, have an essential role in global biogeochemical cycles [...] Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)

Research

Jump to: Editorial

15 pages, 1348 KiB  
Article
Effect of Sub-Stoichiometric Fe(III) Amounts on LCFA Degradation by Methanogenic Communities
by Ana J. Cavaleiro, Ana P. Guedes, Sérgio A. Silva, Ana L. Arantes, João C. Sequeira, Andreia F. Salvador, Diana Z. Sousa, Alfons J. M. Stams and M. Madalena Alves
Microorganisms 2020, 8(9), 1375; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8091375 - 07 Sep 2020
Cited by 6 | Viewed by 2558
Abstract
Long-chain fatty acids (LCFA) are common contaminants in municipal and industrial wastewater that can be converted anaerobically to methane. A low hydrogen partial pressure is required for LCFA degradation by anaerobic bacteria, requiring the establishment of syntrophic relationships with hydrogenotrophic methanogens. However, high [...] Read more.
Long-chain fatty acids (LCFA) are common contaminants in municipal and industrial wastewater that can be converted anaerobically to methane. A low hydrogen partial pressure is required for LCFA degradation by anaerobic bacteria, requiring the establishment of syntrophic relationships with hydrogenotrophic methanogens. However, high LCFA loads can inhibit methanogens, hindering biodegradation. Because it has been suggested that anaerobic degradation of these compounds may be enhanced by the presence of alternative electron acceptors, such as iron, we investigated the effect of sub-stoichiometric amounts of Fe(III) on oleate (C18:1 LCFA) degradation by suspended and granular methanogenic sludge. Fe(III) accelerated oleate biodegradation and hydrogenotrophic methanogenesis in the assays with suspended sludge, with H2-consuming methanogens coexisting with iron-reducing bacteria. On the other hand, acetoclastic methanogenesis was delayed by Fe(III). These effects were less evident with granular sludge, possibly due to its higher initial methanogenic activity relative to suspended sludge. Enrichments with close-to-stoichiometric amounts of Fe(III) resulted in a microbial community mainly composed of Geobacter, Syntrophomonas, and Methanobacterium genera, with relative abundances of 83–89%, 3–6%, and 0.2–10%, respectively. In these enrichments, oleate was biodegraded to acetate and coupled to iron-reduction and methane production, revealing novel microbial interactions between syntrophic LCFA-degrading bacteria, iron-reducing bacteria, and methanogens. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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15 pages, 1506 KiB  
Article
Assessing the Effect of Humic Substances and Fe(III) as Potential Electron Acceptors for Anaerobic Methane Oxidation in a Marine Anoxic System
by Sigrid van Grinsven, Jaap S. Sinninghe Damsté and Laura Villanueva
Microorganisms 2020, 8(9), 1288; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8091288 - 24 Aug 2020
Cited by 11 | Viewed by 2942
Abstract
Marine anaerobic methane oxidation (AOM) is generally assumed to be coupled to sulfate reduction, via a consortium of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). ANME-1 are, however, often found as single cells, or only loosely aggregated with SRB, suggesting they perform [...] Read more.
Marine anaerobic methane oxidation (AOM) is generally assumed to be coupled to sulfate reduction, via a consortium of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). ANME-1 are, however, often found as single cells, or only loosely aggregated with SRB, suggesting they perform a form of AOM independent of sulfate reduction. Oxidized metals and humic substances have been suggested as potential electron acceptors for ANME, but up to now, AOM linked to reduction of these compounds has only been shown for the ANME-2 and ANME-3 clades. Here, the effect of the electron acceptors anthraquinone-disulfonate (AQDS), a humic acids analog, and Fe3+ on anaerobic methane oxidation were assessed by incubation experiments with anoxic Black Sea water containing ANME-1b. Incubation experiments with 13C-methane and AQDS showed a stimulating effect of AQDS on methane oxidation. Fe3+ enhanced the ANME-1b abundance but did not substantially increase methane oxidation. Sodium molybdate, which was added as an inhibitor of sulfate reduction, surprisingly enhanced methane oxidation, possibly related to the dominant abundance of Sulfurospirillum in those incubations. The presented data suggest the potential involvement of ANME-1b in AQDS-enhanced anaerobic methane oxidation, possibly via electron shuttling to AQDS or via interaction with other members of the microbial community. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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13 pages, 1417 KiB  
Article
EMS-Induced Mutagenesis of Clostridium carboxidivorans for Increased Atmospheric CO2 Reduction Efficiency and Solvent Production
by Naoufal Lakhssassi, Azam Baharlouei, Jonas Meksem, Scott D. Hamilton-Brehm, David A. Lightfoot, Khalid Meksem and Yanna Liang
Microorganisms 2020, 8(8), 1239; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8081239 - 14 Aug 2020
Cited by 8 | Viewed by 2698
Abstract
Clostridium carboxidivorans (P7) is one of the most important solvent-producing bacteria capable of fermenting syngas (CO, CO2, and H2) to produce chemical commodities when grown as an autotroph. This study aimed to develop ethyl methanesulfonate (EMS)-induced P7 mutants that [...] Read more.
Clostridium carboxidivorans (P7) is one of the most important solvent-producing bacteria capable of fermenting syngas (CO, CO2, and H2) to produce chemical commodities when grown as an autotroph. This study aimed to develop ethyl methanesulfonate (EMS)-induced P7 mutants that were capable of growing in the presence of CO2 as a unique source of carbon with increased solvent formation and atmospheric CO2 reduction to limit global warming. Phenotypic analysis including growth and end product characterization of the P7 wild type (WT) demonstrated that this strain grew better at 25 °C than 37 °C when CO2 served as the only source of carbon. In the current study, 55 mutagenized P7-EMS mutants were developed by using 100 mM and 120 mM EMS. Interestingly, using a forward genetic approach, three out of the 55 P7-EMS mutants showed a significant increase in ethanol, butyrate, and butanol production. The three P7-EMS mutants presented on average a 4.68-fold increase in concentrations of ethanol when compared to the P7-WT. Butyric acid production from 3 P7-EMS mutants contained an average of a 3.85 fold increase over the levels observed in the P7-WT cultures under the same conditions (CO2 only). In addition, one P7-EMS mutant presented butanol production (0.23 ± 0.02 g/L), which was absent from the P7-WT under CO2 conditions. Most of the P7-EMS mutants showed stability of the obtained end product traits after three transfers. Most importantly, the amount of reduced atmospheric CO2 increased up to 8.72 times (0.21 g/Abs) for ethanol production and up to 8.73 times higher (0.16 g/Abs) for butyrate than the levels contained in the P7-WT. Additionally, to produce butanol, the P7-EMSIII-J mutant presented 0.082 g/Abs of CO2 reduction. This study demonstrated the feasibility and effectiveness of employing EMS mutagenesis in generating solvent-producing anaerobic bacteria mutants with improved and novel product formation and increased atmospheric CO2 reduction efficiency. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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14 pages, 2768 KiB  
Article
Genomic Characterization and Environmental Distribution of a Thermophilic Anaerobe Dissulfurirhabdus thermomarina SH388T Involved in Disproportionation of Sulfur Compounds in Shallow Sea Hydrothermal Vents
by Maxime Allioux, Stéven Yvenou, Galina Slobodkina, Alexander Slobodkin, Zongze Shao, Mohamed Jebbar and Karine Alain
Microorganisms 2020, 8(8), 1132; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8081132 - 27 Jul 2020
Cited by 11 | Viewed by 2488
Abstract
Marine hydrothermal systems are characterized by a pronounced biogeochemical sulfur cycle with the participation of sulfur-oxidizing, sulfate-reducing and sulfur-disproportionating microorganisms. The diversity and metabolism of sulfur disproportionators are studied to a much lesser extent compared with other microbial groups. Dissulfurirhabdus thermomarina SH388T [...] Read more.
Marine hydrothermal systems are characterized by a pronounced biogeochemical sulfur cycle with the participation of sulfur-oxidizing, sulfate-reducing and sulfur-disproportionating microorganisms. The diversity and metabolism of sulfur disproportionators are studied to a much lesser extent compared with other microbial groups. Dissulfurirhabdus thermomarina SH388T is an anaerobic thermophilic bacterium isolated from a shallow sea hydrothermal vent. D. thermomarina is an obligate chemolithoautotroph able to grow by the disproportionation of sulfite and elemental sulfur. Here, we present the results of the sequencing and analysis of the high-quality draft genome of strain SH388T. The genome consists of a one circular chromosome of 2,461,642 base pairs, has a G + C content of 71.1 mol% and 2267 protein-coding sequences. The genome analysis revealed a complete set of genes essential to CO2 fixation via the reductive acetyl-CoA (Wood-Ljungdahl) pathway and gluconeogenesis. The genome of D. thermomarina encodes a complete set of genes necessary for the dissimilatory reduction of sulfates, which are probably involved in the disproportionation of sulfur. Data on the occurrences of Dissulfurirhabdus 16S rRNA gene sequences in gene libraries and metagenome datasets showed the worldwide distribution of the members of this genus. This study expands our knowledge of the microbial contribution into carbon and sulfur cycles in the marine hydrothermal environments. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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22 pages, 2337 KiB  
Article
Pontiella desulfatans gen. nov., sp. nov., and Pontiella sulfatireligans sp. nov., Two Marine Anaerobes of the Pontiellaceae fam. nov. Producing Sulfated Glycosaminoglycan-like Exopolymers
by Daan M. van Vliet, Yuemei Lin, Nicole J. Bale, Michel Koenen, Laura Villanueva, Alfons J. M. Stams and Irene Sánchez-Andrea
Microorganisms 2020, 8(6), 920; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8060920 - 18 Jun 2020
Cited by 11 | Viewed by 4382
Abstract
Recently, we isolated two marine strains, F1T and F21T, which together with Kiritimatiella glycovorans L21-Fru-ABT are the only pure cultures of the class Kiritimatiellae within the phylum Verrucomicrobiota. Here, we present an in-depth genome-guided characterization of both isolates with [...] Read more.
Recently, we isolated two marine strains, F1T and F21T, which together with Kiritimatiella glycovorans L21-Fru-ABT are the only pure cultures of the class Kiritimatiellae within the phylum Verrucomicrobiota. Here, we present an in-depth genome-guided characterization of both isolates with emphasis on their exopolysaccharide synthesis. The strains only grew fermentatively on simple carbohydrates and sulfated polysaccharides. Strains F1T, F21T and K. glycovorans reduced elemental sulfur, ferric citrate and anthraquinone-2,6-disulfonate during anaerobic growth on sugars. Both strains produced exopolysaccharides during stationary phase, probably with intracellularly stored glycogen as energy and carbon source. Exopolysaccharides included N-sulfated polysaccharides probably containing hexosamines and thus resembling glycosaminoglycans. This implies that the isolates can both degrade and produce sulfated polysaccharides. Both strains encoded an unprecedently high number of glycoside hydrolase genes (422 and 388, respectively), including prevalent alpha-L-fucosidase genes, which may be necessary for degrading complex sulfated polysaccharides such as fucoidan. Strain F21T encoded three putative glycosaminoglycan sulfotransferases and a putative sulfate glycosaminoglycan biosynthesis gene cluster. Based on phylogenetic and chemotaxonomic analyses, we propose the taxa Pontiella desulfatans F1T gen. nov., sp. nov. and Pontiella sulfatireligans F21T sp. nov. as representatives of the Pontiellaceae fam. nov. within the class Kiritimatiellae. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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20 pages, 3184 KiB  
Article
Butyrate Conversion by Sulfate-Reducing and Methanogenic Communities from Anoxic Sediments of Aarhus Bay, Denmark
by Derya Ozuolmez, Elisha K. Moore, Ellen C. Hopmans, Jaap S. Sinninghe Damsté, Alfons J. M. Stams and Caroline M. Plugge
Microorganisms 2020, 8(4), 606; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8040606 - 22 Apr 2020
Cited by 9 | Viewed by 3683
Abstract
The conventional perception that the zone of sulfate reduction and methanogenesis are separated in high- and low-sulfate-containing marine sediments has recently been changed by studies demonstrating their co-occurrence in sediments. The presence of methanogens was linked to the presence of substrates that are [...] Read more.
The conventional perception that the zone of sulfate reduction and methanogenesis are separated in high- and low-sulfate-containing marine sediments has recently been changed by studies demonstrating their co-occurrence in sediments. The presence of methanogens was linked to the presence of substrates that are not used by sulfate reducers. In the current study, we hypothesized that both groups can co-exist, consuming common substrates (H2 and/or acetate) in sediments. We enriched butyrate-degrading communities in sediment slurries originating from the sulfate, sulfate–methane transition, and methane zone of Aarhus Bay, Denmark. Sulfate was added at different concentrations (0, 3, 20 mM), and the slurries were incubated at 10 °C and 25 °C. During butyrate conversion, sulfate reduction and methanogenesis occurred simultaneously. The syntrophic butyrate degrader Syntrophomonas was enriched both in sulfate-amended and in sulfate-free slurries, indicating the occurrence of syntrophic conversions at both conditions. Archaeal community analysis revealed a dominance of Methanomicrobiaceae. The acetoclastic Methanosaetaceae reached high relative abundance in the absence of sulfate, while presence of acetoclastic Methanosarcinaceae was independent of the sulfate concentration, temperature, and the initial zone of the sediment. This study shows that there is no vertical separation of sulfate reducers, syntrophs, and methanogens in the sediment and that they all participate in the conversion of butyrate. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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20 pages, 8633 KiB  
Article
Propionate Converting Anaerobic Microbial Communities Enriched from Distinct Biogeochemical Zones of Aarhus Bay, Denmark under Sulfidogenic and Methanogenic Conditions
by Derya Ozuolmez, Alfons J. M. Stams and Caroline M. Plugge
Microorganisms 2020, 8(3), 394; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8030394 - 11 Mar 2020
Cited by 11 | Viewed by 3474
Abstract
The relationship between predominant physiological types of prokaryotes in marine sediments and propionate degradation through sulfate reduction, fermentation, and methanogenesis was studied in marine sediments. Propionate conversion was assessed in slurries containing sediment from three different biogeochemical zones of Aarhus Bay, Denmark. Sediment [...] Read more.
The relationship between predominant physiological types of prokaryotes in marine sediments and propionate degradation through sulfate reduction, fermentation, and methanogenesis was studied in marine sediments. Propionate conversion was assessed in slurries containing sediment from three different biogeochemical zones of Aarhus Bay, Denmark. Sediment slurries were amended with 0, 3, or 20 mM sulfate and incubated at 25 °C and 10 °C for 514–571 days. Methanogenesis in the sulfate zone and sulfate reduction in the methane zone slurries was observed. Both processes occurred simultaneously in enrichments originating from samples along the whole sediment. Bacterial community analysis revealed the dominance of Desulfobacteraceae and Desulfobulbaceae members in sulfate-amended slurries incubated at 25°C and 10°C. Cryptanaerobacter belonging to the Peptococcaceae family dominated sulfate-free methanogenic slurries at 25°C, whereas bacteria related to Desulfobacteraceae were dominant at 10°C. Archaeal community analysis revealed the prevalence of different genera belonging to Methanomicrobiales in slurries incubated at different temperatures and amended with different sulfate concentrations. Methanosarcinaceae were only detected in the absence of sulfate. In summary, Aarhus Bay sediment zones contain sulfate reducers, syntrophs, and methanogens interacting with each other in the conversion of propionate. Our results indicate that in Aarhus Bay sediments, Cryptanaerobacter degraded propionate in syntrophic association with methanogens. Full article
(This article belongs to the Special Issue Anaerobes in Biogeochemical Cycles)
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