Title Long-Term Warming Effects on the Microbiome and Nitrogen Fixation

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Title Long-Term Warming Effects on the Microbiome and Nitrogen Fixation bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Title Long-term warming effects on the microbiome and nitrogen 2 fixation associated with the moss Racomitrium lanuginosum in a 3 subarctic alpine heathland 4 Running title Shifts in a moss microbiome after 20 years warming 5 Ingeborg J. Klarenberg1,2, Christoph Keuschnig3, Ana J. Russi Colmenares2, Anne D. Jungblut4, 6 Ingibjörg S. Jónsdóttir2, Oddur Vilhelmsson1,5,6 7 1Natural Resource Sciences, University of Akureyri, Borgir i Nordurslod, 600 Akureyri, Iceland 8 2Faculty of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavík, 9 Iceland 10 3Environmental Microbial Genomics, Laboratoire Ampère, CNRS, École Centrale de Lyon, 11 Écully, France 12 4Life Sciences Department, The Natural History Museum, London, United Kingdom 13 5BioMedical Center, University of Iceland, Reykjavík, Iceland 14 6School of Biological Sciences, University of Reading, Reading, United Kingdom 15 Corresponding author: 16 Ingeborg J. Klarenberg 17 Borgir i Nordurslod, 600 Akureyri, Iceland 18 [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 19 Abstract 20 Bacterial communities form the basis of biogeochemical processes and determine 21 plant growth and health. Mosses, an abundant plant group in many Arctic ecosystems, 22 harbour diverse bacterial communities that are for instance involved in nitrogen fixation. 23 Global climate change is causing changes in aboveground plant biomass and shifting 24 species composition in the Arctic, but little is known about the response of the moss 25 microbiome. Here, we study the bacterial community associated with the moss 26 Racomitrium lanuginosum, a common species in the Arctic, in a 20-year in situ warming 27 experiment in an Icelandic heathland. We evaluate changes in bacterial community 28 composition and diversity. Further, we assess the consequences of warming for nifH 29 gene copy numbers and nitrogen fixation rates. Our findings indicate an increase in the 30 relative abundance of Proteobacteria and a decrease in the relative abundance of 31 Cyanobacteria and Acidobacteria with warming. The nifH gene copy number decreases, 32 while the rate of nitrogen fixation is not affected. This contradiction could be explained 33 by a shift in the nitrogen fixing bacterial community. Although climate warming might 34 not change the contribution of R. lanuginosum to nitrogen input in nitrogen-limited 35 ecosystems, the microbial community resilience and the nitrogen fixing taxa may shift. 2 bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 36 Introduction 37 Temperature in high-latitude regions is rising twice as fast as elsewhere [1], which 38 has large impacts on Arctic ecosystems, for instance by altering species distributions and 39 interactions among species [2, 3]. One such interaction that might be affected by warming 40 is the interaction between mosses and their associated bacterial communities and related 41 ecosystem processes. 42 Mosses comprise a large component of the vegetation in many high-latitude 43 ecosystems and play important roles in biogeochemical cycles by forming a carbon (C) 44 sink via their slow decomposition rates, by accounting for up to 7% of terrestrial net 45 primary productivity and half of the terrestrial nitrogen (N2) fixation [4–8]. Most mosses 46 consist of a upper living segment with photosynthetic tissue and a lower decaying dead 47 segment and thus link above-ground and belowground processes [9]. They provide a 48 habitat for a range of microbiota, micro- and mesofauna, which together with the alive and 49 dead moss tissue have been defined as the ‘bryosphere’ [10]. Moss-associated 50 microorganisms are involved in the decomposition of dead moss tissue and responsible for 51 N2 fixation. N2 fixation by Cyanobacteria associated with mosses directly increases moss 52 growth rates [11] and thereby controls C sequestration in moss tissues. These 53 Cyanobacteria are also an important source of new available N in boreal and Arctic 54 ecosystems [12, 13]. In order to understand the implications of climate change for the role 55 of mosses in ecosystem C and N cycling, we need to understand how moss-associated 56 microbial communities react to elevated temperatures. 57 The bacterial community composition of mosses is species specific and influenced 58 by environmental factors such as pH and nutrient availability [14–16]. Bacterial associates 59 can increase mosses survival and growth under extreme conditions [17], for instance by 3 bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 60 protecting moss tissue from freeze damage [18]. Commonly found phyla associated with 61 mosses are Proteobacteria, Acidobacteria, Actinobacteria, Bacteroidetes, 62 Armatimonadetes, Verrucomicrobia, Planctomycetes and Cyanobacteria [16, 19]. While 63 Cyanobacteria have received most of the attention for their N2-fixing capability [11, 20– 64 26], mosses harbour many other putative N2-fixing (diazotrophic) taxa such as members 65 of the Alphaproteobacteria [14, 27–29]. The bacterial community composition of mosses 66 has primarily been studied for peat and feather mosses, but we know little about the 67 bacterial communities of other moss species. 68 N2 fixation rates of moss-associated diazotrophic bacteria can be expected to 69 increase with temperature, as metabolic processes in microorganisms increase with 70 temperature and the enzyme nitrogenase is more active at higher temperatures [30]. 71 Temperature induced drought however, can inhibit N2 fixation rates, especially 72 cyanobacterial N2 fixation [9, 24, 31–36]. Temperature effects on N2 fixation rates might 73 also be influenced by physiological adaptation of diazotrophic communities, or shifts to a 74 species composition better suited to the new conditions [31, 37, 38]. Despite the 75 importance of microbial communities for plant functioning and ecosystem processes, the 76 effect of warming on moss microbial communities has received little attention. Two studies 77 describing warming related changes in peat moss bacterial community composition 78 reported a decrease in overall bacterial and diazotrophic diversity with higher temperatures 79 in situ and under laboratory conditions [39, 40]. Whether this warming induced decrease 80 in diversity also holds for bacterial communities associated with other moss species in high 81 latitudes is unknown. Moreover, long-term warming effects on moss-associated bacterial 82 communities have yet to be explored. 4 bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 83 In this study we investigated how two decades of experimental warming with open 84 top chambers impact the bacterial community and N2 fixation rates associated with the 85 moss Racomitrium lanuginosum (Hedw.) Brid in a subarctic-alpine dwarf shrub heath in 86 northern Iceland. R. lanuginosum has a wide distribution at high altitudes in temperate 87 regions of the Northern and Southern Hemisphere and at low altitudes in the Arctic [41]. 88 Projected temperature increases for Iceland as a whole are estimated between 2.1 to 4.0 89 degrees °C by 2100 [42]. 90 We assessed the bacterial community composition by 16S rRNA gene amplicon 91 sequencing and we hypothesised (1) that long-term warming would reduce the bacterial 92 richness and diversity and affect community composition as compared to non-warmed 93 control plots. N2 fixation rates were measured with acetylene reduction assays (ARA) and 94 N2 fixation potential was quantified by quantitative PCR (qPCR) of nitrogenase (nifH) 95 genes. We hypothesised (2) that N2 fixation would be either positively or negatively 96 influenced by long-term warming depending on the warming-induced changes in the 97 abundance of potential N2-fixing taxa. 98 Methods 99 Field site 100 The sampling was conducted in permanent plots of a long-term warming simulation 101 experiment, part of the International Tundra Experiment (ITEX), in northwest Iceland [43]. 102 According to Köppen’s climate definitions, the sampling site, called Auðkúluheiði 103 (65°16’N, 20°15’W, 480 m above sea level) is situated in the lower Arctic. The vegetation 104 has been characterized as a relatively species-rich dwarf shrub heath, with Betula nana 105 being the most dominant vascular species and the moss R. lanuginosum and the lichen 5 bioRxiv preprint doi: https://doi.org/10.1101/838581; this version posted November 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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