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A song of ice and mud: Interactions of microbes with roots, fauna and carbon in warming permafrost-affected soils
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. (Climate Impacts Research Centre)ORCID iD: 0000-0001-9923-2036
2018 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Sagan om is och gyttja: interaktioner mellan mikrober och rötter, fauna och kol när permafrost-påverkade marker värms upp (Swedish)
Abstract [en]

Permafrost-affected soils store a large quantity of soil organic matter (SOM) – ca. half of worldwide soil carbon – and currently undergo rapid and severe warming due to climate change. Increased SOM decomposition by microorganisms and soil fauna due to climate change, poses the risk of a positive climate feedback through the release of greenhouse gases. Direct effects of climate change on SOM decomposition, through such mechanisms as deepening of the seasonally-thawing active layer and increasing soil temperatures, have gathered considerable scientific attention in the last two decades. Yet, indirect effects mediated by changes in plant, microbial, and fauna communities, remain poorly understood. Microbial communities, which may be affected by climate change-induced changes in vegetation composition or rooting patterns, and may in turn affect SOM decomposition, are the primary focus of the work described in this thesis.

We used (I) a field-scale permafrost thaw experiment in a palsa peatland, (II) a laboratory incubation of Yedoma permafrost with inoculation by exotic microorganisms, (III) a microcosm experiment with five plant species grown either in Sphagnum peat or in newly-thawed permafrost peat, and (IV) a field-scale cold season warming experiment in cryoturbated tundra to address the indirect effects of climate change on microbial drivers of SOM decomposition. Community composition data for bacteria and fungi were obtained by amplicon sequencing and phospholipid fatty acid extraction, and for collembola by Tullgren extraction, alongside measurements of soil chemistry, CO2 emissions and root density.

We showed that in situ thawing of a palsa peatland caused colonization of permafrost soil by overlying soil microbes. Further, we observed that functional limitations of permafrost microbial communities can hamper microbial metabolism in vitro. Relieving these functional limitations in vitro increased cumulative CO2 emissions by 32% over 161 days and introduced nitrification. In addition, we found that different plant species did not harbour different rhizosphere bacterial communities in Sphagnum peat topsoil, but did when grown in newly-thawed permafrost peat. Plant species may thus differ in how they affect functional limitations in thawing permafrost soil. Therefore, climate change-induced changes in vegetation composition might alter functioning in the newly-thawed, subsoil permafrost layer of northern peatlands, but less likely so in the topsoil. Finally, we observed that vegetation encroachment in barren cryoturbated soil, due to reduced cryogenic activity with higher temperatures, change both bacterial and collembola community composition, which may in turn affect soil functioning.

This thesis shows that microbial community dynamics and plant-decomposer interactions play an important role in the functioning of warming permafrost-affected soils. More specifically, it demonstrates that the effects of climate change on plants can trickle down on microbial communities, in turn affecting SOM decomposition in thawing permafrost.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2018. , p. 37
Keywords [en]
microbial communities, permafrost, functional limitations, rhizosphere, SOM decomposition, soil fauna, climate change, carbon dioxide
National Category
Ecology Environmental Sciences Climate Research Microbiology Geochemistry
Identifiers
URN: urn:nbn:se:umu:diva-151472ISBN: 978-91-7601-928-3 (print)OAI: oai:DiVA.org:umu-151472DiVA, id: diva2:1245131
Public defence
2018-09-28, N430, Naturvetarhuset, Umeå, 10:15 (English)
Opponent
Supervisors
Funder
Knut and Alice Wallenberg Foundation, KAW 2012.0152Swedish Research Council Formas, Dnr 214-2011-788Swedish Research Council, Dnr 621-2011-5444Available from: 2018-09-07 Created: 2018-09-04 Last updated: 2018-09-05Bibliographically approved
List of papers
1. Long-term in situ permafrost thaw effects on bacterial communities and potential aerobic respiration
Open this publication in new window or tab >>Long-term in situ permafrost thaw effects on bacterial communities and potential aerobic respiration
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2018 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 12, no 9, p. 2129-2141Article in journal (Refereed) Published
Abstract [en]

The decomposition of large stocks of soil organic carbon in thawing permafrost might depend on more than climate change-induced temperature increases: indirect effects of thawing via altered bacterial community structure (BCS) or rooting patterns are largely unexplored. We used a 10-year in situ permafrost thaw experiment and aerobic incubations to investigate alterations in BCS and potential respiration at different depths, and the extent to which they are related with each other and with root density. Active layer and permafrost BCS strongly differed, and the BCS in formerly frozen soils (below the natural thawfront) converged under induced deep thaw to strongly resemble the active layer BCS, possibly as a result of colonization by overlying microorganisms. Overall, respiration rates decreased with depth and soils showed lower potential respiration when subjected to deeper thaw, which we attributed to gradual labile carbon pool depletion. Despite deeper rooting under induced deep thaw, root density measurements did not improve soil chemistry-based models of potential respiration. However, BCS explained an additional unique portion of variation in respiration, particularly when accounting for differences in organic matter content. Our results suggest that by measuring bacterial community composition, we can improve both our understanding and the modeling of the permafrost carbon feedback.

Place, publisher, year, edition, pages
Springer Nature, 2018
National Category
Ecology Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-151468 (URN)10.1038/s41396-018-0176-z (DOI)000441581700003 ()29875436 (PubMedID)2-s2.0-85048074422 (Scopus ID)
Note

A correction to this article has been published. DOI: 10.1038/s41396-019-0384-1

Available from: 2018-09-04 Created: 2018-09-04 Last updated: 2019-08-12Bibliographically approved
2. Permafrost microbial community composition limits C and N cycling
Open this publication in new window or tab >>Permafrost microbial community composition limits C and N cycling
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(English)Manuscript (preprint) (Other academic)
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-151469 (URN)
Available from: 2018-09-04 Created: 2018-09-04 Last updated: 2018-09-05
3. Permafrost peatland plant rhizobiome: limited effects of plant presence in Sphagnum peat contrast with strong, species-specific effects in newly-thawed permafrost
Open this publication in new window or tab >>Permafrost peatland plant rhizobiome: limited effects of plant presence in Sphagnum peat contrast with strong, species-specific effects in newly-thawed permafrost
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Sphagnum peatlands in the permafrost region store large amounts of carbon. Changes in plant communities or increasing CO2 concentrations may alter rhizodeposition and in turn soil carbon cycling, yet the response of rhizosphere processes to climate change is insufficiently understood. Microbial communities in the rhizosphere – the rhizobiome – may be important in determining the rates of such processes, and often depend on both soil types and plant species. Sphagnum peat is very acidic and contains numerous secondary metabolites, which may override rhizodeposits effects on the rhizobiome, while newly-thawed, but more decomposed permafrost peat layers may be more favourable to the formation of a distinct rhizobiome. These two soil types may thus have different sensitivities to plant community-driven shifts in microbial communities. However, plant species effects on the bacterial rhizobiome have never been investigated in Sphagnum peat and in newly-thawed permafrost.We grew five vascular peatland plant species, abundant across the circum-arctic and encompassing different plant functional and mycorrhizal types, in Sphagnum peat or in newly-thawed permafrost peat, and compared their bacterial rhizobiome to communities in non-planted controls. The rhizobiome of three plant species out of five was not distinct from non-planted Sphagnum peat, while only the rhizobiome of Andromeda polifolia and, to a lesser extent, Rubus chamaemorus were distinct. In contrast, in newly-thawed permafrost soil, all five plant species had a rhizobiome distinct from non-planted controls, and also exhibited plant species-specific differences. While the differences between rhizosphere and non-planted newly-thawed permafrost soil were overall similar between plant species at the phylum-level, many of the OTUs that differed were specific to a single plant species, particularly so for B. nana and E. vaginatum. The small or absence of  differences between the rhizobiomes and Sphagnum peat for most plant species is likely due to acidity and Sphagnum secondary metabolites. Changes in aboveground vegetation may therefore not affect soil processes in Sphagnum peat through altered bacterial communities. In contrast, the strong and plant species-specific effects on the rhizobiome in newly-thawed permafrost soil is due to either less constraining conditions or because permafrost bacterial communities are more vulnerable to rhizosphere effects. Deep-rooting plants can colonize newly-thawed permafrost, and even shallow-rooting species can do so after soil mixing events that bring thawed permafrost to the surface. Therefore, different bacterial communities can be expected depending on permafrost thaw scenario and existing plant community. Plant roots of different species may thus differ in their effects on carbon and nutrient cycling in newly-thawed permafrost not only through differing rhizodeposits but also through species-specific rhizobiomes.

National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-151470 (URN)
Available from: 2018-09-04 Created: 2018-09-04 Last updated: 2018-09-05
4. Microbial and soil fauna diversity responses to winter climate change and greening in cryoturbated arctic tundra
Open this publication in new window or tab >>Microbial and soil fauna diversity responses to winter climate change and greening in cryoturbated arctic tundra
(English)Manuscript (preprint) (Other academic)
Abstract [en]

At high latitudes, winter warming facilitates vegetation expansion into barren frost-affected soils. The interplay of changes in winter climate and plant presence may alter soil carbon dynamics via effects on decomposers. Responses of decomposer soil fauna and microorganisms to such changes likely differ from each other, since their life histories, dispersal mechanisms and microhabitats vary greatly. We investigated the relative impacts of short-term winter warming and long-term increases in plant cover on bacteria and collembola community composition in cryoturbated, non-sorted circle (NSC) tundra. By covering NSCs with insulating gardening fiber cloth (fleeces) or using stone walls accumulating snow, we imposed two climate-change scenarios: snow accumulation increased autumn-to-late winter soil temperatures by 1.4°C, while fleeces warmed soils during that period by 1°C and increased spring temperatures by 1.1°C. Summer bacteria and collembola communities were sampled from within-circle locations differing in vegetation abundance and soil properties, representing stages in long-term NSC overgrowth. Two years of winter warming had no effects on both decomposer communities. Instead, their community compositions were strongly determined by sampling location: communities in barren circle centers were distinct from those in vegetated outer rims, while communities in sparsely vegetated patches of circle centers were intermediate. Diversity patterns indicate that collembola communities are tightly linked to plant presence while bacteria communities correlated with soil properties. Our results thus suggest that short-term effects of winter warming are likely to be minimal, but longer-term vegetation overgrowth of NSCs affects decomposer community composition substantially. At decadal timescales, collembola community changes may follow rapidly after plant establishment into barren areas, whereas bacteria communities may take longer to respond. If shifts in decomposer community composition are indicative for changes in their decomposition activity, vegetation overgrowth will likely have much stronger effects on carbon losses from frost-affected tundra than short-term winter warming.

National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-151471 (URN)
Available from: 2018-09-04 Created: 2018-09-04 Last updated: 2018-09-05

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