The nitrogen cycle in cryoconites: naturally occurring nitrification‐denitrification granules on a glacier

Segawa, Tomio; Ishii, Satoshi; Ohte, Nobuhito; Akiyoshi, Ayumi; Yamada, Akinori; Maruyama, Fumito; Li, Zhongqin; Hongoh, Yuichi; Takeuchi, Nozomu

doi:10.1111/1462-2920.12543

Cited by 76 publications

(74 citation statements)

References 68 publications

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“…We found that N cycling functional gene abundances increased with time, which was in agreement with previous research in Tianshan Mountain No.1 glacier, showing that N cycling functional gene abundances increased along the chronosequence (Segawa et al, 2014). However, Brankatschk et al (2011) showed that ammonia oxidizing microbial community abundances increased with time, but denitrifying bacterial ( nirK/S and nosZ ) gene abundances decreased in the Damma Glacier forefield.…”

Section: Discussionsupporting

confidence: 92%

“…Segawa et al (2014) found isotope ratio evidence of the occurrence of nitrification on the surface of the Tianshan Mountain No.1 glacier. Past research indicated that in the glacier foreland ecosystem the ammonia-oxidizing process was mainly driven by AOA, due to the AOA having a better adaptability to the ammonia-poor environment and lower pH than AOB (Di et al, 2009; Ollivier et al, 2011).…”

Section: Discussionmentioning

confidence: 95%

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Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China

et al. 2016

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Structural succession and its driving factors for nitrogen (N) cycling microbial communities during the early stages of soil development (0–44 years) were studied along a chronosequence in the glacial forelands of the Tianshan Mountain No.1 glacier in the arid and semi-arid region of central Asia. We assessed the abundance and population of functional genes affiliated with N-fixation (nifH), nitrification (bacterial and archaeal amoA), and denitrification (nirK/S and nosZ) in a glacier foreland using molecular methods. The abundance of functional genes significantly increased with soil development. N cycling community compositions were also significantly shifted within 44 years and were structured by successional age. Cyanobacterial nifH gene sequences were the most dominant N fixing bacteria and its relative abundance increased from 56.8–93.2% along the chronosequence. Ammonia-oxidizing communities shifted from the Nitrososphaera cluster (AOA-amoA) and the Nitrosospira cluster ME (AOB-aomA) in younger soils (0 and 5 years) to communities dominated by soil and sediment 1 (AOA-amoA) and Nitrosospira Cluster 2 Related (AOB-aomA) in older soils (≥17 years). Most of the denitrifers closest relatives were potential aerobic denitrifying bacteria, and some other types of denitrifying bacteria (like autotrophic nitrate-reducing, sulfide-oxidizing bacteria and denitrifying phosphorus removing bacteria) were also detected in all soil samples. The regression analysis showed that N cycling microbial communities were dominant in younger soils (0–5 years) and significantly correlated with soil total carbon, while communities that were most abundant in older soils were significantly correlated with soil total nitrogen. These results suggested that the shift of soil C and N contents during the glacial retreat significantly influenced the abundance, composition and diversity of N cycling microbial communities.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 95%

Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China

et al. 2016

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“…High abundance of cyanobacteria has been already observed in polar and alpine cryoconite (Segawa et al, 2014;Stibal et al, 2014), whereas low abundance was reported on Rotmoosferner Glacier (Tirol, Austria; Edwards et al, 2013). Consistently, coverage of psbD (photosystem II P680 reaction center D2 protein gene) was (mean ± s.e.)…”

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confidence: 58%

Light-dependent microbial metabolisms drive carbon fluxes on glacier surfaces

et al. 2016

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Biological processes on glacier surfaces affect glacier reflectance, influence surface energy budget and glacier response to climate warming, and determine glacier carbon exchange with the atmosphere. Currently, carbon balance of supraglacial environment is assessed as the balance between the activity of oxygenic phototrophs and the respiration rate of heterotrophic organisms. Here we present a metagenomic analysis of tiny wind-blown supraglacial sediment (cryoconite) from Baltoro (Pakistani Karakoram) and Forni (Italian Alps) glaciers, providing evidence for the occurrence in these environments of different and previously neglected metabolic pathways. Indeed, we observed high abundance of heterotrophic anoxygenic phototrophs, suggesting that light might directly supplement the energy demand of some bacterial strains allowing them to use as carbon source organic molecules, which otherwise would be respired. Furthermore, data suggest that CO 2 could be produced also by microbiologically mediated oxidation of CO, which may be produced by photodegradation of organic matter. The ISME Journal Climate change is determining a global cryosphere shrinkage and mountain glacier environments are declining (IPPC, 2014). The consequent loss of biodiversity is yet to be fully assessed, particularly the loss of functional biodiversity in extreme environments (Stibal et al., 2012;Boetius et al., 2015). Cryoconite holes, that is, small depressions on glacier surfaces whose formation is because of windborne debris (cryoconite), are the most biologically active environments on glaciers (Boetius et al., 2015).We used whole-metagenomic sequencing to investigate the main functions of six cryoconite holes from Forni (Italian Alps) and six from Baltoro (Pakistani Karakoram) glaciers. We focused on carbon and energy metabolisms by comparing the total coverage of marker genes for photosynthesis, use of inorganic and organic compounds as energy source and autotrophy/heterotrophy. We also used metagenomic sequences for the taxonomic attribution of microorganisms carrying specific metabolic genes Table S4 reports the marker genes whose coverage (mean number per base of reads mapping the genes) was used to infer the abundance of each metabolism. Supplementary Table S5 and Figure 1 report their normalized coverages. Finally, we measured chemical/physical parameters of cryoconite holes and oxygen consumption rates on the days of sampling, both under light and dark conditions (Supplementary Table S3 and Supplementary Figure S2). The main hypothesis tested was whether oxygenic phototrophy and organotrophic respiration represent the only significant metabolisms affecting carbon balance on glacier surface, as currently conceived, or other microbial processes could contribute to it.On the basis of 16S rRNA gene sequencing, Cyanobacteria represented 22 and 3% of the microbial community on Forni and Baltoro, respectively (Supplementary Figure S3). High abundance of cyanobacteria has been already observed in polar and alpine cryoconite (Segawa et al....

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“…In several other environments, such phenomena have been explained by anoxic microhabitats, created by biofilm formation and oxygen depletion by aerobes [8]. Indeed, denitrification processes were detected in cryoconite granules that were less than 2 mm in diameter, where Polaromonas cells have been proposed as O 2 scavengers and extracellular polymer producers, causing clumping of the sediment [26]. Polaromonas spp.…”

Section: Discussionmentioning

confidence: 99%

Enrichment of Cryoconite Hole Anaerobes: Implications for the Subglacial Microbiome

et al. 2016

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Glaciers have recently been recognized as ecosystems comprised of several distinct habitats: a sunlit and oxygenated glacial surface, glacial ice, and a dark, mostly anoxic glacial bed. Surface meltwaters annually flood the subglacial sediments by means of drainage channels. Glacial surfaces host aquatic microhabitats called cryoconite holes, regarded as “hot spots” of microbial abundance and activity, largely contributing to the meltwaters’ bacterial diversity. This study presents an investigation of cryoconite hole anaerobes and discusses their possible impact on subglacial microbial communities, combining 16S rRNA gene fragment amplicon sequencing and the traditional enrichment culture technique. Cryoconite hole sediment harbored bacteria belonging mainly to the Proteobacteria (21%), Bacteroidetes (16%), Actinobacteria (14%), and Planctomycetes (6%) phyla. An 8-week incubation of those sediments in Postgate C medium for sulfate reducers in airtight bottles, emulating subglacial conditions, eliminated a great majority of dominant taxa, leading to enrichment of the Firmicutes (62%), Proteobacteria (14%), and Bacteroidetes (13%), which consisted of anaerobic genera like Clostridium, Psychrosinus, Paludibacter, and Acetobacterium. Enrichment of Pseudomonas spp. also occurred, suggesting it played a role as a dominant oxygen scavenger, providing a possible scenario for anaerobic niche establishment in subglacial habitats. To our knowledge, this is the first paper to provide insight into the diversity of the anaerobic part of the cryoconite hole microbial community and its potential to contribute to matter turnover in anoxic, subglacial sites.

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The nitrogen cycle in cryoconites: naturally occurring nitrification‐denitrification granules on a glacier

Cited by 76 publications

References 68 publications

Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China

Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China

Light-dependent microbial metabolisms drive carbon fluxes on glacier surfaces

Enrichment of Cryoconite Hole Anaerobes: Implications for the Subglacial Microbiome

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