Similar heterotrophic communities but distinct interactions supported by red and green-snow algae in the Antarctic Peninsula.

Antarctic bacteria and fungi climate warming community structure microbial interaction snow algae

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
02 2022
Historique:
received: 30 05 2021
accepted: 17 09 2021
pubmed: 5 10 2021
medline: 25 3 2022
entrez: 4 10 2021
Statut: ppublish

Résumé

Snow algae are predicted to expand in polar regions due to climate warming, which can accelerate snowmelt by reducing albedo. Green snow frequently occurs near penguin colonies, and red snow distributes widely along ocean shores. However, the mechanisms underpinning the assemblage of algae and heterotrophs in colored snow remain poorly characterized. We investigated algal, bacterial, and fungal communities and their interactions in red and green snows in the Antarctic Peninsula using a high-throughput sequencing method. We found distinct algal community structure in red and green snows, and the relative abundance of dominant taxa varied, potentially due to nutrient status differences. Contrastingly, red and green snows exhibited similar heterotrophic communities (bacteria and fungi), whereas the relative abundance of fungal pathogens was substantially higher in red snow by 3.8-fold. Red snow exhibited a higher network complexity, indicated by a higher number of nodes and edges. Red snow exhibited a higher proportion of negative correlations among heterotrophs (62.2% vs 3.4%) and stronger network stability, suggesting the red-snow network is more resistant to external disturbance. Our study revealed that the red snow microbiome exhibits a more stable microbial network than the green snow microbiome.

Identifiants

pubmed: 34606623
doi: 10.1111/nph.17764
doi:

Banques de données

RefSeq
['MW136658', 'FM955256']
figshare
['10.6084/m9.figshare.14980716', '10.6084/m9.figshare.14980710', '10.6084/m9.figshare.14891346']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1358-1368

Informations de copyright

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.

Références

Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM. 2009. A method for studying protistan diversity using massively parallel sequencing of v9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4: e6372.
Apprill A, McNally S, Parsons R, Weber L. 2015. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquatic Microbial Ecology 75: 129-137.
Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F et al. 2013. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution 4: 914-919.
Benomar S, Ranava D, Cárdenas ML, Trably E, Rafrafi Y, Ducret A, Hamelin J, Lojou E, Steyer J-P, Giudici-Orticoni M-T. 2015. Nutritional stress induces exchange of cell material and energetic coupling between bacterial species. Nature Communications 6: e7283.
Bidigare RR, Ondrusek ME, Kennicutt MC, Iturriaga R, Harvey HR, Hoham RW, Macko SA. 1993. Evidence for a photoprotective function for secondary carotenoids of snow algae. Journal of Phycology 29: 427-434.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. Blast+: architecture and applications. BMC Bioinformatics 10: e421.
Clarke KR, Warwick RM. 2006. Primer v.6: user manual/tutorial. Plymouth, UK: Primer-E.
Coyte KZ, Schluter J, Foster KR. 2015. The ecology of the microbiome: networks, competition, and stability. Science 350: 663-666.
Csardi G, Nepusz T. 2006. The igraph software package for complex network research. InterJournal Complex Systems 1695(5): 1-9.
Davey MP, Norman L, Sterk P, Huete-Ortega M, Bunbury F, Loh BKW, Stockton S, Peck LS, Convey P, Newsham KK et al. 2019. Snow algae communities in Antarctica: metabolic and taxonomic composition. New Phytologist 222: 1242-1255.
Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, Bastida F, Berhe AA, Cutler NA, Gallardo A et al. 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution 4: 210-220.
Edgar RC. 2016. Unoise2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. doi: 10.1101/081257.
Edgar RC. 2018. Accuracy of taxonomy prediction for 16S rRNA and fungal ITS sequences. PeerJ 6: e4652.
Faust K, Raes J. 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology 10: 538-550.
Faust K, Raes J. 2016. CoNet app: inference of biological association networks using Cytoscape. F1000Research 5: e1519.
Fontaine C, Guimarães PR Jr., Kéfi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thébault E. 2011. The ecological and evolutionary implications of merging different types of networks. Ecology Letters 14: 1170-1181.
Fujii M, Takano Y, Kojima H, Hoshino T, Tanaka R, Fukui M. 2010. Microbial community structure, pigment composition, and nitrogen source of red snow in Antarctica. Microbial Ecology 59: 466-475.
Gálvez FE, Saldarriaga-Córdoba M, Huovinen P, Silva AX, Gómez I. 2021. Revealing the characteristics of the Antarctic snow alga Chlorominima collina gen. et sp. nov. through taxonomy, physiology, and transcriptomics. Frontiers in Plant Science 12: e662298.
Ganey GQ, Loso MG, Burgess AB, Dial RJ. 2017. The role of microbes in snowmelt and radiative forcing on an Alaskan icefield. Nature Geoscience 10: 754-759.
Gray A, Krolikowski M, Fretwell P, Convey P, Peck LS, Mendelova M, Smith AG, Davey MP. 2020. Remote sensing reveals Antarctic green snow algae as important terrestrial carbon sink. Nature Communications 11: e2527.
Hamilton TL, Havig J. 2017. Primary productivity of snow algae communities on stratovolcanoes of the Pacific Northwest. Geobiology 15: 280-295.
Hernandez DJ, David AS, Menges ES, Searcy CA, Afkhami ME. 2021. Environmental stress destabilizes microbial networks. The ISME Journal 15: 1722-1734.
Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE et al. 2012. New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82: 666-677.
Kagami M, de Bruin A, Ibelings BW, Van Donk E. 2007. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578: 113-129.
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
Khan A, Kong W, Ji M, Yue L, Xie Y, Liu J, Xu B. 2020. Disparity in soil bacterial community succession along a short time-scale deglaciation chronosequence on the Tibetan Plateau. Soil Ecology Letters 2: 83-92.
Kim BK, Joo H, Lee B, Lee D-H, Ahn I-Y, Ha S-Y. 2018. Physiological characteristics and related biochemical parameters of snow algae from King George Island, Antarctica. Ocean Science Journal 53: 621-630.
Kounosu A, Murase K, Yoshida A, Maruyama H, Kikuchi T. 2019. Improved 18S and 28S rDNA primer sets for NGS-based parasite detection. Scientific Reports 9: e15789.
Krug L, Erlacher A, Markut K, Berg G, Cernava T. 2020. The microbiome of alpine snow algae shows a specific inter-kingdom connectivity and algae-bacteria interactions with supportive capacities. The ISME Journal 14: 2197-2210.
Legendre P, Anderson MJ. 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs 69: 1-24.
Li YM, Jiang LL, Lv WW, Cui SJ, Zhang LR, Wang Q, Meng FD, Li BW, Liu PP, Suonan J et al. 2019. Fungal pathogens pose a potential threat to animal and plant health in desertified and pika-burrowed alpine meadows on the Tibetan Plateau. Canadian Journal of Microbiology 65: 365-376.
Luo W, Ding H, Li H, Ji Z, Huang K, Zhao W, Yu Y, Zeng Y. 2020. Molecular diversity of the microbial community in coloured snow from the Fildes Peninsula (King George Island, Maritime Antarctica). Polar Biology 43: 1391-1405.
Lutz S, Anesio AM, Edwards A, Benning LG. 2017. Linking microbial diversity and functionality of arctic glacial surface habitats. Environmental Microbiology 19: 551-565.
Lutz S, Anesio AM, Field K, Benning LG. 2015. Integrated ‘omics’, targeted metabolite and single-cell analyses of arctic snow algae functionality and adaptability. Frontiers in Microbiology 6: e1323.
Lutz S, Anesio AM, Jorge Villar SE, Benning LG. 2014. Variations of algal communities cause darkening of a Greenland glacier. FEMS Microbiology Ecology 89: 402-414.
Lutz S, Anesio AM, Raiswell R, Edwards A, Newton RJ, Gill F, Benning LG. 2016. The biogeography of red snow microbiomes and their role in melting arctic glaciers. Nature Communications 7: e11968.
Matsen FA, Kodner RB, Armbrust EV. 2010. Pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11: e538.
Netotea S, Pongor S. 2006. Evolution of robust and efficient system topologies. Cellular Immunology 244: 80-83.
Newman MEJ. 2003. The structure and function of complex networks. Siam Review 45: 167-256.
Nguyen N, Song Z, Bates S, Branco S, Tedersoo L, Menke J, Schilling J, Kennedy P. 2015. FunGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20: 241-248.
Parada AE, Needham DM, Fuhrman JA. 2016. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology 18: 1403-1414.
Peng G-S, Tan S-Y, Wu J, Holme P. 2016. Trade-offs between robustness and small-world effect in complex networks. Scientific Reports 6: e37317.
Price MN, Dehal PS, Arkin AP. 2010. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490.
Procházková L, Leya T, Křížková H, Nedbalová L. 2019. Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): the taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow. FEMS Microbiology Ecology 95: fiz064.
Procházková L, Remias D, Bilger W, Křížkoví H, Řezanka T, Nedbalová L. 2020. Cysts of the snow alga Chloromonas krienitzii (Chlorophyceae) show increased tolerance to ultraviolet radiation and elevated visible light. Frontiers in Plant Science 11: e617250.
Pruesse E, Peplies J, Glöckner FO. 2012. Sina: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
Remias D, Jost S, Boenigk J, Wastian J, Lütz C. 2013a. Hydrurus-related golden algae (Chrysophyceae) cause yellow snow in polar summer snowfields. Psychological Research Psychologische Forschung 61: 277-285.
Remias D, Lutz-Meindl U, Lütz C. 2005. Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. European Journal of Phycology 40: 259-268.
Remias D, Wastian H, Lütz C, Leya T. 2013b. Insights into the biology and phylogeny of Chloromonas polyptera (Chlorophyta), an alga causing orange snow in Maritime Antarctica. Antarctic Science 25: 648-656.
Rodrigues MV, Müller T, Buchheim MA, Canbäck B, Wolf M. 2017. THESES db: the algae 18S rDNA sequence-structure database for inferring phylogenies. Phycologia 56: 186-192.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ et al. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537-7541.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13: 2498-2504.
Soto DF, Fuentes R, Huovinen P, Gomez I. 2020. Microbial composition and photosynthesis in Antarctic snow algae communities: integrating metabarcoding and pulse amplitude modulation fluorometry. Algal Research 45: e101738.
Stamatakis A. 2014. RAxML v.8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, Richards TA. 2010. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Microbial Ecology 19: 21-31.
Taylor LH, Latham SM, Woolhouse ME. 2001. Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 356: 983-989.
Van den Wyngaert S, Rojas-Jimenez K, Seto K, Kagami M, Grossart H-P. 2018. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. Journal of Eukaryotic Microbiology 65: 870-881.
Wardeh M, Risley C, McIntyre MK, Setzkorn C, Baylis M. 2015. Database of host-pathogen and related species interactions, and their global distribution. Scientific Data 2: e150049.
Watts DJ, Strogatz SH. 1998. Collective dynamics of ‘small-world’ networks. Nature 393: 440-442.
White TJ, Bruns T, Lee S, Taylor J, eds. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. San Diego, CA, USA: Academic Press, 317.
Wirth F, Goldani LZ. 2012. Epidemiology of Rhodotorula: an emerging pathogen. Interdisciplinary Perspectives on Infectious Diseases 2012: e465717.
Yuan MM, Guo X, Wu L, Zhang YA, Xiao N, Ning D, Shi Z, Zhou X, Wu L, Yang Y et al. 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change 11: 343-348.
Yue L, Kong W, Ji M, Liu J, Morgan-Kiss RM. 2019. Community response of microbial primary producers to salinity is primarily driven by nutrients in lakes. Science of the Total Environment 696: e134001.
Zhu R, Wang Q, Ding W, Wang C, Hou L, Ma D. 2014. Penguins significantly increased phosphine formation and phosphorus contribution in maritime Antarctic soils. Scientific Reports 4: e7055.

Auteurs

Mukan Ji (M)

Key Laboratory of Alpine Ecology, Institute of Tibetan Plateau Research, Chinese Academy of Sciences (CAS), Beijing, 100101, China.

Weidong Kong (W)

Key Laboratory of Alpine Ecology, Institute of Tibetan Plateau Research, Chinese Academy of Sciences (CAS), Beijing, 100101, China.
University of Chinese Academy of Sciences, Beijing, 100039, China.
CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences, Beijing, 100101, China.

Hongzeng Jia (H)

Key Laboratory of Alpine Ecology, Institute of Tibetan Plateau Research, Chinese Academy of Sciences (CAS), Beijing, 100101, China.
University of Chinese Academy of Sciences, Beijing, 100039, China.

Chen Ding (C)

The Association of Science Education Promotion of China, Beijing, 100083, China.

Alexandre M Anesio (AM)

Department of Environmental Science, Aarhus University, Roskilde, DK-4000, Denmark.

Yanfen Wang (Y)

University of Chinese Academy of Sciences, Beijing, 100039, China.
CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences, Beijing, 100101, China.

Yong-Guan Zhu (YG)

State Key Laboratory of Urban and Reginal Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH