In proglacial floodplains, glacier recession promotes biogeochemical and ecological gradients across relatively small spatial scales. The resulting environmental heterogeneity induces remarkable microbial biodiversity among proglacial stream biofilms. Yet the relative importance of environmental constraints in forming biofilm communities remains largely unknown. Extreme environmental conditions in proglacial streams may lead to the homogenizing selection of biofilm-forming microorganisms. However, environmental differences between proglacial streams may impose different selective forces, resulting in nested, spatially structured assembly processes. Here, we investigated bacterial community assembly processes by unraveling ecologically successful phylogenetic clades in two stream types (glacier-fed mainstems and non-glacier-fed tributaries) draining three proglacial floodplains in the Swiss Alps. Clades with low phylogenetic turnover rates were present in all stream types, including Gammaproteobacteria and Alphaproteobacteria, while the other clades were specific to one stream type. These clades constituted up to 34.8% and 31.1% of the community diversity and up to 61.3% and 50.9% of the relative abundances in mainstems and tributaries, respectively, highlighting their importance and success in these communities. Furthermore, the proportion of bacteria under homogeneous selection was inversely related to the abundance of photoautotrophs, and these clades may therefore decrease in abundance with the future "greening" of proglacial habitats. Finally, we found little effect of physical distance from the glacier on clades under selection in glacier-fed streams, probably due to the high hydrological connectivity of our study reaches. Overall, these findings shed new light on the mechanisms of microbial biofilm assembly in proglacial streams and help us to predict their future in a rapidly changing environment. IMPORTANCE Streams draining proglacial floodplains harbor benthic biofilms comprised of diverse microbial communities. These high-mountain ecosystems are rapidly changing with climate warming, and it is therefore critical to better understand the mechanisms underlying the assembly of their microbial communities. We found that homogeneous selection dominates the structuring of bacterial communities in benthic biofilms in both glacier-fed mainstems and nonglacier tributary streams within three proglacial floodplains in the Swiss Alps. However, differences between glacier-fed and tributary ecosystems may impose differential selective forces. Here, we uncovered nested, spatially structured assembly processes for proglacial floodplain communities. Our analyses additionally provided insights into linkages between aquatic photoautotrophs and the bacterial taxa under homogeneous selection, potentially by providing a labile source of carbon in these otherwise carbon-deprived systems. In the future, we expect a shift in the bacterial communities under homogeneous selection in glacier-fed streams as primary production becomes more important and streams become "greener".

Department of Ecology Faculty of Science Charles University Prague Czechia

Group AlpWISE Institute of Earth Surface Dynamics University of Lausanne Lausanne Switzerland

River Ecosystems Laboratory Ecole Polytechnique Fédérale de Lausanne Lausanne Switzerland

Systems Ecology Group Luxembourg Centre for Systems Biomedicine University of Luxembourg Esch sur Alzette Luxembourg

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Carrivick JL, Heckmann T, Turner A, Fischer M. 2018. An assessment of landform composition and functioning with the first proglacial systems dataset of the central European Alps. Geomorphology 321:117–128. 10.1016/j.geomorph.2018.08.030. DOI

Anderson SP. 2007. Biogeochemistry of glacial landscape systems. Annu Rev Earth Planet Sci 35:375–399. 10.1146/annurev.earth.35.031306.140033. DOI

Heckmann T, McColl S, Morche D. 2016. Retreating ice: research in pro-glacial areas matters. Earth Surf Process Landf 41:271–276. 10.1002/esp.3858. DOI

Bormann BT, Sidle RC. 1990. Changes in productivity and distribution of nutrients in a chronosequence at Glacier Bay National Park, Alaska. J Ecol 78:561–578. 10.2307/2260884. DOI

Ficetola GF, Marta S, Guerrieri A, Gobbi M, Ambrosini R, Fontaneto D, Zerboni A, Poulenard J, Caccianiga M, Thuiller W. 2021. Dynamics of ecological communities following current retreat of glaciers. Annu Rev Ecol Evol Syst 52:405–426. 10.1146/annurev-ecolsys-010521-040017. DOI

Miller HR, Lane SN. 2019. Biogeomorphic feedbacks and the ecosystem engineering of recently deglaciated terrain. Prog Phys Geogr 43:24–45. 10.1177/0309133318816536. DOI

Malard F, Tockner K, Ward JV. 2000. Physico-chemical heterogeneity in a glacial riverscape. Landsc Ecol 15:679–695. 10.1023/A:1008147419478. DOI

Brown LE, Milner AM, Hannah DM. 2007. Groundwater influence on alpine stream ecosystems. Freshw Biol 52:878–890. 10.1111/j.1365-2427.2007.01739.x. DOI

Brown LE, Hannah DM, Milner AM. 2003. Alpine stream habitat classification: an alternative approach incorporating the role of dynamic water source contributions. Arct Antarct Alp Res 35:313–322. 10.1657/1523-0430(2003)035[0313:ASHCAA]2.0.CO;2. DOI

Ward JV. 1994. Ecology of alpine streams. Freshw Biol 32:277–294. 10.1111/j.1365-2427.1994.tb01126.x. DOI

Uehlinger U, Robinson CT, Hieber M, Zah R. 2010. The physico-chemical habitat template for periphyton in alpine glacial streams under a changing climate, p 107–121. In Stevenson RJ, Sabater S (ed), Global change and river ecosystems—implications for structure, function and ecosystem services. Springer, Dordrecht, Netherlands.

Gabbud C, Bakker M, Clémençon M, Lane SN. 2019. Hydropower flushing events cause severe loss of macrozoobenthos in alpine streams. Water Resour Res 55:10056–10081. 10.1029/2019WR024758. DOI

Milner AM, Petts GE. 1994. Glacial rivers: physical habitat and ecology. Freshw Biol 32:295–307. 10.1111/j.1365-2427.1994.tb01127.x. DOI

Milner AM, Brittain JE, Brown LE, Hannah DM. 2010. Water sources and habitat of alpine streams, p 175–191. In Bundi U (ed), Alpine waters. The handbook of environmental chemistry. Springer, Berlin, Germany.

Milner AM, Khamis K, Battin TJ, Brittain JE, Barrand NE, Füreder L, Cauvy-Fraunié S, Gíslason GM, Jacobsen D, Hannah DM, Hodson AJ, Hood E, Lencioni V, Ólafsson JS, Robinson CT, Tranter M, Brown LE. 2017. Glacier shrinkage driving global changes in downstream systems. Proc Natl Acad Sci USA 114:9770–9778. 10.1073/pnas.1619807114. PubMed DOI PMC

Battin TJ, Wille A, Sattler B, Psenner R. 2001. Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microbiol 67:799–807. 10.1128/AEM.67.2.799-807.2001. PubMed DOI PMC

Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K. 2013. Microbial biodiversity in glacier-fed streams. ISME J 7:1651–1660. 10.1038/ismej.2013.44. PubMed DOI PMC

Brandani J, Peter H, Busi SB, Kohler TJ, Fodelianakis S, Ezzat L, Michoud G, Bourquin M, Pramateftaki P, Roncoroni M, Lane SN, Battin TJ. 2022. Spatial patterns of benthic biofilm diversity among streams draining proglacial floodplains. Front Microbiol 13:948165. 10.3389/fmicb.2022.948165. PubMed DOI PMC

Vellend M, Cornwell WK, Magnuson-Ford K, Mooers AO. 2010. Measuring phylogenetic biodiversity, p 194–207. In Magurran AE, McGill BJ (ed), Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, United Kingdom.

Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka AE. 2013. Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. 10.1038/ismej.2013.93. PubMed DOI PMC

Stegen JC, Lin X, Fredrickson JK, Konopka AE. 2015. Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol 6:370. 10.3389/fmicb.2015.00370. PubMed DOI PMC

Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF. 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA 112:E1326–E1332. 10.1073/pnas.1414261112. PubMed DOI PMC

Ezzat L, Fodelianakis S, Kohler TJ, Massimo B, Brandani J, Busi SB, Daffonchio D, de Staercke V, Marasco R, Michoud G, Oppliger E, Peter H, Pramateftaki P, Schön M, Styllas M, Tadei V, Tolosano M, Battin TJ. 2022. Benthic biofilms in glacier-fed streams from Scandinavia to the Himalayas host distinct bacterial communities compared with the streamwater. Appl Environ Microbiol 88:e00421-22. 10.1128/aem.00421-22. PubMed DOI PMC

Fodelianakis S, Washburne AD, Bourquin M, Pramateftaki P, Kohler TJ, Styllas M, Tolosano M, de Staercke V, Schön M, Busi SB, Brandani J, Wilmes P, Peter H, Battin TJ. 2022. Microdiversity characterizes prevalent phylogenetic clades in the glacier-fed stream microbiome. ISME J 16:666–675. 10.1038/s41396-021-01106-6. PubMed DOI PMC

Kohler TJ, Fodelianakis S, Michoud G, Ezzat L, Bourquin M, Peter H, Busi SB, Pramateftaki P, Deluigi N, Styllas M, Tolosano M, de Staercke V, Schön M, Brandani J, Marasco R, Daffonchio D, Wilmes P, Battin TJ. 2022. Glacier shrinkage will accelerate downstream decomposition of organic matter and alters microbiome structure and function. Glob Chang Biol 28:3846–3859. 10.1111/gcb.16169. PubMed DOI PMC

Busi SB, Bourquin M, Fodelianakis S, Michoud G, Kohler TJ, Peter H, Pramateftaki P, Styllas M, Tolosano M, de Staercke V, Schön M, de Nies L, Marasco R, Daffonchio D, Ezzat L, Wilmes P, Battin TJ. 2022. Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams. Nat Commun 13:2168. 10.1038/s41467-022-29914-0. PubMed DOI PMC

Allen R, Hoffmann LJ, Larcombe MJ, Louisson Z, Summerfield TC. 2020. Homogeneous environmental selection dominates microbial community assembly in the oligotrophic South Pacific Gyre. Mol Ecol 29:4680–4691. 10.1111/mec.15651. PubMed DOI

Li Y, Gao Y, Zhang W, Wang C, Wang P, Niu L, Wu H. 2019. Homogeneous selection dominates the microbial community assembly in the sediment of the Three Gorges Reservoir. Sci Total Environ 690:50–60. 10.1016/j.scitotenv.2019.07.014. PubMed DOI

Zhang K, Shi Y, Cui X, Yue P, Li K, Liu X, Tripathi BM, Chu H. 2019. Salinity is a key determinant for soil microbial communities in a desert ecosystem. mSystems 4:e00225-18. 10.1128/mSystems.00225-18. PubMed DOI PMC

Vass M, Székely AJ, Lindström ES, Langenheder S. 2020. Using null models to compare bacterial and microeukaryotic metacommunity assembly under shifting environmental conditions. Sci Rep 10:2455. 10.1038/s41598-020-59182-1. PubMed DOI PMC

Freimann R, Bürgmann H, Findlay SEG, Robinson CT. 2013. Bacterial structures and ecosystem functions in glaciated floodplains: contemporary states and potential future shifts. ISME J 7:2361–2373. 10.1038/ismej.2013.114. PubMed DOI PMC

Kohler TJ, Peter H, Fodelianakis S, Pramateftaki P, Styllas M, Tolosano M, de Staercke V, Schön M, Busi SB, Wilmes P, Washburne AD, Battin TJ. 2020. Patterns and drivers of extracellular enzyme activity in New Zealand glacier-fed streams. Front Microbiol 11:591465. 10.3389/fmicb.2020.591465. PubMed DOI PMC

Uehlinger U, Zah R, Bürgi HR. 1998. The Val Roseg project: temporal and spatial patterns of benthic algae in an alpine stream ecosystem influenced by glacier runoff. Hydrology 429–424.

Rott E, Cantonati M, Füreder L, Pfister P. 2006. Benthic algae in high altitude streams of the Alps—a neglected component of the aquatic biota. Hydrobiologia 562:195–216. 10.1007/s10750-005-1811-z. DOI

Battin TJ, Besemer K, Bengtsson MM, Romaní AM, Packman AI. 2016. The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol 14:251–263. 10.1038/nrmicro.2016.15. PubMed DOI

Kohler TJ, Vinšová P, Falteisek L, Žárský JD, Yde JC, Hatton JE, Hawkings JR, Lamarche-Gagnon G, Hood E, Cameron KA, Stibal M. 2020. Patterns in microbial assemblages exported from the meltwater of Arctic and sub-Arctic glaciers. Front Microbiol 11:669. 10.3389/fmicb.2020.00669. PubMed DOI PMC

Darcy JL, Lynch RC, King AJ, Robeson MS, Schmidt SK. 2011. Global distribution of Polaromonas phylotypes—evidence for a highly successful dispersal capacity. PLoS One 6:e23742. 10.1371/journal.pone.0023742. PubMed DOI PMC

Smith HJ, Foreman CM, Ramaraj T. 2014. Draft genome sequence of a metabolically diverse Antarctic supraglacial stream organism, Polaromonas sp. strain CG9_12, determined using Pacific Biosciences single-molecule real-time sequencing technology. Genome Announc 2:e01242-14. 10.1128/genomeA.01242-14. PubMed DOI PMC

Blois J, Williams JW, Fitzpatrick MC, Jackson ST, Ferrier S. 2013. Space can substitute for time in predicting climate-change effects on biodiversity. Proc Natl Acad Sci USA 110:9374–9379. 10.1073/pnas.1220228110. PubMed DOI PMC

Rickenbacher M. 2013. Journeys through time with the Swiss national map series.

Raup B, Racoviteanu A, Khalsa SJS, Helm C, Armstrong R, Arnaud Y. 2007. The GLIMS geospatial glacier database: a new tool for studying glacier change. Glob Planet Change 56:101–110. 10.1016/j.gloplacha.2006.07.018. DOI

Linsbauer A, Huss M, Hodel E, Bauder A, Fischer M, Weidmann Y, Bärtschi H, Schmassmann E. 2021. The new Swiss glacier inventory SGI2016: from a topographical to a glaciological dataset. Front Earth Sci (Lausanne) 9:704189. 10.3389/feart.2021.704189. DOI

Busi SB, Pramateftaki P, Brandani J, Fodelianakis S, Peter H, Halder R, Wilmes P, Battin TJ. 2020. Optimised biomolecular extraction for metagenomic analysis of microbial biofilms from high-mountain streams. PeerJ 8:e9973. 10.7717/peerj.9973. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. 10.1093/bioinformatics/btu170. PubMed DOI PMC

Boylen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, et al. . 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. 10.1038/s41587-019-0209-9. PubMed DOI PMC

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. 10.1038/nmeth.3869. PubMed DOI PMC

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and Web-based tools. Nucleic Acids Res 41:D590–D596. 10.1093/nar/gks1219. PubMed DOI PMC

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. 10.1093/bioinformatics/btq166. PubMed DOI

Washburne AD, Silverman JD, Leff JW, Bennett DJ, Darcy JL, Mukherjee S, Fierer N, David LA. 2017. Phylogenetic factorization of compositional data yields lineage-level associations in microbiome datasets. PeerJ 5:e2969. 10.7717/peerj.2969. PubMed DOI PMC

Washburne AD, Silverman JD, Morton JT, Becker DJ, Crowley D, Mukherjee S, David LA, Plowright RK. 2019. Phylofactorization: a graph partitioning algorithm to identify phylogenetic scales of ecological data. Ecol Monogr 89:e01353. 10.1002/ecm.1353. DOI

Gu Z, Eils R, Schlesner M. 2016. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32:2847–2849. 10.1093/bioinformatics/btw313. PubMed DOI

McMurdie PJ, Holmes S. 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. 10.1371/journal.pone.0061217. PubMed DOI PMC

R Core Team. 2021. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.