Lake Bacterial Communities in North Patagonian Andes: The Effect of the Nothofagus pumilio Treeline.
Nothofagus pumilio forest
Bacterial community composition
Krummholz belt
Phylogenetic clustering
Species turnover
Treeline
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
09 Oct 2024
09 Oct 2024
Historique:
received:
03
07
2024
accepted:
02
10
2024
medline:
9
10
2024
pubmed:
9
10
2024
entrez:
8
10
2024
Statut:
epublish
Résumé
One of the most noticeable environmental discontinuities in mountains is the transition that exists in vegetation below and above the treeline. In the North Patagonian Andean lakes (between 900 and 1950 m a.s.l.), we analyzed the bacterial community composition of lakes in relation to surrounding vegetation (erected trees, krummholz belt, and bare rocks), dissolved organic carbon (DOC), and total dissolved nutrients (nitrogen, TDN and phosphorus, TDP). We observed a decrease in DOC, TDP, and TDN concentrations with altitude, reflecting shifts in the source inputs entering the lakes by runoff. Cluster analysis based on bacterial community composition showed a segregation of the lakes below treeline, from those located above. This first cluster was characterized by the cyanobacteria Cyanobium PCC-6307, while in the krummholz belt and bare rocks, bacterial communities were dominated by Actinobacteria hgcl-clade and Proteobacteria (Sandarakinorhabdus and Rhodovarius), with the presence of pigments such as actinorhodopsin, carotenoids, and bacteriochlorophyll a. The net relatedness index (NRI), which considers the community phylogenetic dispersion, showed that lakes located on bare rocks were structured by environmental filtering, while communities of lakes below treeline were structured by species interactions such as competition. Beta-diversity was higher among lakes below than among lakes located above the treeline. The contribution of species turnover was more important than nestedness. Our study brings light on how bacterial communities may respond to changes in the surrounding vegetation, highlighting the importance of evaluating different aspects of community structure to understand metacommunity organization.
Identifiants
pubmed: 39379544
doi: 10.1007/s00248-024-02443-7
pii: 10.1007/s00248-024-02443-7
doi:
Substances chimiques
Nitrogen
N762921K75
Carbon
7440-44-0
Phosphorus
27YLU75U4W
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
123Subventions
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT 2015-2138
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT 2017-1940
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT 2018-1563
Informations de copyright
© 2024. The Author(s).
Références
Moser KA, Baron JS, Brahney J, Oleksy IA, Saros JE, Hundey EJ, Sadro SA, Kopáček J, Sommaruga R, Kainz MJ, Strecker AL, Chandra S, Walters DM, Preston DL, Michelutti N, Lepori F, Spaulding SA, Christianson KR, Melack JM, Smol JP (2019) Mountain lakes: eyes on global environmental change. Global Planet Change 178:77–95
doi: 10.1016/j.gloplacha.2019.04.001
Williamson CE, Rose KC (2009) Ultraviolet insights: attempting to resolve enigmatic patterns in pelagic freshwaters - the historical context and a view to the future. Int Rev Hydrobiol 94:129–142
doi: 10.1002/iroh.200811099
Catalán N, Rofner C, Verpoorter C, Pérez MT, Dittmar T, Tranvik L, Sommaruga R, Peter H (2024) Treeline displacement may affect lake dissolved organic matter processing at high latitudes and altitudes. Nat Commun 15:2640
pubmed: 38531850
pmcid: 10965997
doi: 10.1038/s41467-024-46789-5
Harsch MA, Hulme PE, McGlone MS, Duncan RP (2009) Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12:1040–1049
pubmed: 19682007
doi: 10.1111/j.1461-0248.2009.01355.x
Zheng X, Babst F, Camarero JJ, Li X, Lu X, Gao S, Sigdel SR, Wang Y, Zhu H, Liang E (2024) Density-dependent species interactions modulate alpine treeline shifts. Ecol Lett 27:e14403
pubmed: 38577961
doi: 10.1111/ele.14403
Rofner C, Peter H, Catalán N, Drewes F, Sommaruga R, Pérez MT (2017) Climate-related changes of soil characteristics affect bacterial community composition and function of high altitude and latitude lakes. Global Change Biol 23:2331–2344
doi: 10.1111/gcb.13545
Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, Livingstone DM, Sommaruga R, Straile D, Van Donk E, Weyhenmeyer GA, Winder M (2009) Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–2297
pubmed: 20396409
pmcid: 2854826
doi: 10.4319/lo.2009.54.6_part_2.2283
Tiberti R, Buscaglia F, Callieri C, Rogora M, Tartari G, Sommaruga R (2020) Food web complexity of high mountain lakes is largely affected by glacial retreat. Ecosystems 23:1093–1106
doi: 10.1007/s10021-019-00457-8
Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Trans R Soc Lond B Biol Sci 365:2093–2106
pubmed: 20513717
pmcid: 2880135
doi: 10.1098/rstb.2010.0055
Dullinger S, Dirnböck T, Grabherr G (2004) Modelling climate change-driven treeline shifts: relative effects of temperature increase, dispersal and invasibility. J Ecol 92:241–252
doi: 10.1111/j.0022-0477.2004.00872.x
Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28
pubmed: 21070562
doi: 10.1111/j.1461-0248.2010.01552.x
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecol Biogeogr 19:134–143
doi: 10.1111/j.1466-8238.2009.00490.x
Baselga A (2013) Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol Evol 4:552–557
doi: 10.1111/2041-210X.12029
Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Global Ecol Biogeogr 23:1324–1334
doi: 10.1111/geb.12207
Dobrovolski R, Melo AS, Cassemiro FA, Diniz-Filho JAF (2012) Climatic history and dispersal ability explain the relative importance of turnover and nestedness components of beta diversity. Global Ecol Biogeogr 21:191–197
doi: 10.1111/j.1466-8238.2011.00671.x
Fontana V, Guariento E, Hilpold A, Niedrist G, Steinwandter M, Spitale D, Nascimbene J, Tappeiner U, Seeber J (2020) Species richness and beta diversity patterns of multiple taxa along an elevational gradient in pastured grasslands in the European Alps. Sci Rep 10:12516
pubmed: 32719437
pmcid: 7385172
doi: 10.1038/s41598-020-69569-9
Bastidas Navarro M, Balseiro E, Modenutti B (2014) Bacterial community structure in Patagonian Andean Lakes above and below timberline: from community composition to community function. Microb Ecol 68:528–541
pubmed: 24863131
doi: 10.1007/s00248-014-0439-9
Vincent K, Holland-Moritz H, Solon AJ, Gendron EM, Schmidt SK (2022) Crossing treeline: bacterioplankton communities of alpine and subalpine rocky mountain lakes. Front Microbiol 12:533121
pubmed: 35046907
pmcid: 8762171
doi: 10.3389/fmicb.2021.533121
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
doi: 10.1146/annurev.ecolsys.33.010802.150448
Mouquet N, Devictor V, Meynard CN, Munoz F, Bersier LF, Chave J, Couteron P, Dalecky A, Fontaine C, Gravel D (2012) Ecophylogenetics: advances and perspectives. Biol Rev 87:769–785
pubmed: 22432924
doi: 10.1111/j.1469-185X.2012.00224.x
Hildebrand-Vogel R, Godoy R, Vogel A (1990) Subantarctic-Andean Nothofagus pumilio forests. Vegetatio 89:55–68
doi: 10.1007/BF00134434
Daniels LD, Veblen TT (2004) Spatiotemporal influences of climate on altitudinal treeline in northern Patagonia. Ecology 85:1284–1296
doi: 10.1890/03-0092
Fajardo A (2018) Insights into intraspecific wood density variation and its relationship to growth, height and elevation in a treeline species. Plant Biol 20:456–464
pubmed: 29394527
doi: 10.1111/plb.12701
Paruelo JM, Beltrán A, Jobbágy E, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and controls on biotic processes. Ecol Austral 8:085–101
APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, AWWA, Washington, D. C.
Murphy KR, Boehme JR, Brown C, Noble M, Smith G, Sparks D, Ruiz GM (2013) Exploring the limits of dissolved organic matter fluorescence for determining seawater sources and ballast water exchange on the US Pacific coast. J Mar Syst 111–112:157–166
doi: 10.1016/j.jmarsys.2012.10.010
Lawaetz AJ, Stedmon CA (2009) Fluorescence intensity calibration using the Raman scatter peak of water. Appl Spectrosc 63:936–940
pubmed: 19678992
doi: 10.1366/000370209788964548
Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigment determination. Archiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie 14:14–36
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
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Oksanen J (2013) Vegan: ecological diversity. R Proj 368:1–11
Stedmon CA, Bro R (2008) Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnol Oceanogr Methods 6:572–579
doi: 10.4319/lom.2008.6.572
Murphy KR, Stedmon CA, Graeber D, Bro R (2013) Fluorescence spectroscopy and multi-way techniques. PARAFAC Anal Methods 5:6557–6566
doi: 10.1039/c3ay41160e
Murphy KR, Stedmon CA, Wenig P, Bro R (2014) OpenFluor–an online spectral library of auto-fluorescence by organic compounds in the environment. Anal Methods 6:658–661
doi: 10.1039/C3AY41935E
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
doi: 10.1111/j.1442-9993.1993.tb00438.x
Baselga A (2017) Partitioning abundance-based multiple-site dissimilarity into components: balanced variation in abundance and abundance gradients. Methods Ecol Evol 8:799–808
doi: 10.1111/2041-210X.12693
Kembel S (2010) An introduction to the picante package. R Proj 1–16
Srur AM, Villalba R, Rodríguez-Catón M, Amoroso MM, Marcotti E (2018) Climate and Nothofagus pumilio establishment at upper treelines in the Patagonian Andes. Front Earth Sci 6:57
doi: 10.3389/feart.2018.00057
Bastidas Navarro M, Díaz Villanueva V, Modenutti B (2019) High phosphorus content in leachates of the austral beech Nothofagus pumilio stimulates bacterioplankton C-consumption. Freshw Sci 38:435–447
doi: 10.1086/704752
Harsch MA, Bader MY (2011) Treeline form–a potential key to understanding treeline dynamics. Global Ecol Biogeogr 20:582–596
doi: 10.1111/j.1466-8238.2010.00622.x
Ruiz-González C, Archambault E, Laforest-Lapointe I, del Giorgio PA, Kembel SW, Messier C, Nock CA, Beisner BE (2018) Soils associated to different tree communities do not elicit predictable responses in lake bacterial community structure and function. FEMS Microbiol Ecol 94(8):fiy115
doi: 10.1093/femsec/fiy115
Paruelo JM, Beltran A, Jobbagy E, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and controls on biotic processes. Ecol Austral 8:85–101
Selak L, Osterholz H, Stanković I, Hanžek N, Gligora Udovič M, Dittmar T, Orlić S (2022) Adaptations of microbial communities and dissolved organics to seasonal pressures in a mesotrophic coastal Mediterranean lake. Environ Microbiol 24:2282–2298
pubmed: 35106913
doi: 10.1111/1462-2920.15924
de Almeida PIN, de Jesus HE, Pereira PHF, Vieira CED, Bianchini A, Martins CDMG, Dos Santos HF (2023) The microbial profile of rivers and lagoons three years after the impact of the world’s largest mining disaster (Fundão dam, Brazil). Environ Res 216:114710
pubmed: 36334830
doi: 10.1016/j.envres.2022.114710
Blanchette ML, Lund MA (2021) Aquatic ecosystems of the Anthropocene: limnology and microbial ecology of mine pit lakes. Microorganisms 9:1207
pubmed: 34204924
pmcid: 8228816
doi: 10.3390/microorganisms9061207
Callieri C, Coci M, Corno G, Macek M, Modenutti B, Balseiro E, Bertoni R (2013) Phylogenetic diversity of nonmarine picocyanobacteria. FEMS Microbiol Ecol 85:293–301
pubmed: 23528076
doi: 10.1111/1574-6941.12118
Modenutti B, Martyniuk N, Bastidas Navarro M, Balseiro E (2023) Glacial influence affects modularity in bacterial community structure in three deep Andean North-Patagonian lakes. Microb Ecol 86:1869–1880
pubmed: 36735066
doi: 10.1007/s00248-023-02184-z
Callieri C, Cronberg G, Stockner JG (2012) Freshwater picocyanobacteria: single cells, microcolonies and colonial forms. In: Whitton BA (ed) Ecology of Cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 229–269
doi: 10.1007/978-94-007-3855-3_8
Forbes CM, O’Leary ND, Dobson AD, Marchesi JR (2009) The contribution of ‘omic’-based approaches to the study of enhanced biological phosphorus removal microbiology. FEMS Microbiol Ecol 69:1–15
pubmed: 19486153
doi: 10.1111/j.1574-6941.2009.00698.x
Dwulit-Smith JR, Hamilton JJ, Stevenson DM, He S, Oyserman BO, Moya-Flores F, Garcia SL, Amador-Noguez D, McMahon KD, Forest KT (2018) acI Actinobacteria assemble a functional actinorhodopsin with natively synthesized retinal. Appl Environ Microbiol 84:e01678-e1618
pubmed: 30315080
pmcid: 6275354
doi: 10.1128/AEM.01678-18
Zufiaurre A, Felip M, Camarero L, Sala-Faig M, Juhanson J, Bonilla-Rosso G, Hallin S, Catalan J (2022) Bacterioplankton seasonality in deep high-mountain lakes. Front Microbiol 13:935378
pubmed: 36187988
pmcid: 9519062
doi: 10.3389/fmicb.2022.935378
Piwosz K, Vrdoljak A, Frenken T, González-Olalla JM, Šantić D, McKay RM, Spilling K, Guttman L, Znachor P, Mujakić I (2020) Light and primary production shape bacterial activity and community composition of aerobic anoxygenic phototrophic bacteria in a microcosm experiment. mSphere 5(4):10–1128
Čuperová Z, Holzer E, Salka I, Sommaruga R, Koblížek M (2013) Temporal changes and altitudinal distribution of aerobic anoxygenic phototrophs in mountain lakes. Appl Environ Microbiol 79:6439–6446
pubmed: 23956384
pmcid: 3811222
doi: 10.1128/AEM.01526-13
Kämpfer P, Busse H-J, Rosséllo-Mora R, Kjellin E, Falsen E (2004) Rhodovarius lipocyclicus gen. nov. sp. nov., a new genus of the α-1 subclass of the Proteobacteria. Syst Appl Microbiol 27:511–516
pubmed: 15490551
doi: 10.1078/0723202041748235
Gich F, Overmann J (2006) Sandarakinorhabdus limnophila gen. nov., sp. nov., a novel bacteriochlorophyll a-containing, obligately aerobic bacterium isolated from freshwater lakes. Int J Syst Evol Microbiol 56:847–854
pubmed: 16585705
doi: 10.1099/ijs.0.63970-0
Aguilar P, Sommaruga R (2020) The balance between deterministic and stochastic processes in structuring lake bacterioplankton community over time. Mol Ecol 29:3117–3130
pubmed: 32628343
pmcid: 7540538
doi: 10.1111/mec.15538
Shi L, Cai Y, Shi X, Zhang M, Zeng Q, Kong F, Xu P (2022) Community structure of aerobic anoxygenic phototrophic bacteria in algae-and macrophyte-dominated areas in Taihu Lake, China. J Oceanol Limnol 40:1855–1867
doi: 10.1007/s00343-022-1348-2
Shi L, Yuanfeng C, Hualin Y, Peng X, Pengfu L, Lingdong K, Fanxiang K (2009) Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J Environ Sci 21:1581–1590
doi: 10.1016/S1001-0742(08)62459-6
Wirth R, Böjti T, Lakatos G, Maroti G, Bagi Z, Rakhely G, Kovacs KL (2019) Characterization of core microbiomes and functional profiles of mesophilic anaerobic digesters fed with Chlorella vulgaris green microalgae and maize silage. Front Energy Res 7:111
doi: 10.3389/fenrg.2019.00111
Podani J, Schmera D (2016) Once again on the components of pairwise beta diversity. Ecol Inform 32:63–68
doi: 10.1016/j.ecoinf.2016.01.002
Leprieur F, Descombes P, Gaboriau T, Cowman PF, Parravicini V, Kulbicki M, Melián CJ, De Santana CN, Heine C, Mouillot D (2016) Plate tectonics drive tropical reef biodiversity dynamics. Nat Commun 7:11461
pubmed: 27151103
pmcid: 4859061
doi: 10.1038/ncomms11461
Gaston KJ, Davies RG, Orme CDL, Olson VA, Thomas GH, Ding T-S, Rasmussen PC, Lennon JJ, Bennett PM, Owens IPF, Blackburn TM (2007) Spatial turnover in the global avifauna. Proc R Soc Lond B Biol Sci 274:1567–1574
Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960
pubmed: 19702749
doi: 10.1111/j.1461-0248.2009.01354.x
Zhang Y, Zhang H, Dong X, Yue D, Zhou L (2022) Effects of oxidizing environment on digestate humification and identification of substances governing the dissolved organic matter (DOM) transformation process. Front Environ Sci Eng 16:99
doi: 10.1007/s11783-022-1520-0
Dial RJ, Maher CT, Hewitt RE, Sullivan PF (2022) Sufficient conditions for rapid range expansion of a boreal conifer. Nature 608:546–551
pubmed: 35948635
pmcid: 9385489
doi: 10.1038/s41586-022-05093-2
Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manage 259:698–709
doi: 10.1016/j.foreco.2009.09.023