|
|
Meter-scale variation within a single transect demands attention to taxon accumulation curves in riverine microbiome studies |
Bingdi Liu1, Lin Zhang1, Jason H. Knouft2,3, Fangqiong Ling1,4,5,6( ) |
1. Department of Energy, Environmental and Chemical Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA 2. Department of Biology, Saint Louis University, St. Louis, MO 63103, USA 3. National Great Rivers Research and Education Center, East Alton, MO 62035, USA 4. Department of Computer Science and Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA 5. Division of Biological and Biomedical Sciences, Washington University in St. Louis, St. Louis, MO 63110, USA 6. Division of Computational and Data Science, Washington University in St. Louis, St. Louis, MO 63130, USA |
|
|
Abstract ● Riverine microbiomes exhibited hyperlocal variation within a single transect. ● Certain family-level taxa directionally associated with river center and bank. ● Taxon accumulation curves within a transect urges more nuanced sampling design. Microbial communities inhabiting river ecosystems play crucial roles in global biogeochemical cycling and pollution attenuation. Spatial variations in local microbial assemblages are important for detailed understanding of community assembly and developing robust biodiversity sampling strategies. Here, we intensely analyzed twenty water samples collected from a one-meter spaced transect from the near-shore to the near-center in the Meramec River in eastern Missouri, USA and examined the microbial community composition with 16S rRNA gene amplicon sequencing. Riverine microbiomes across the transect exhibited extremely high similarity, with Pearson’s correlation coefficients above 0.9 for all pairwise community composition comparisons. However, despite the high similarity, PERMANOVA revealed significant spatial differences between near-shore and near-center communities (p = 0.001). Sloan’s neutral model simulations revealed that within-transect community composition variation was largely explained by demographic stochasticity (R2 = 0.89). Despite being primarily explained by neutral processes, LefSe analyses also revealed taxa from ten families of which relative abundances differed directionally from the bank to the river center, indicating an additional role of environmental filtering. Notably, the local variations within a river transect can have profound impacts on the documentation of alpha diversity. Taxon-accumulation curves indicated that even twenty samples did not fully saturate the sampling effort at the genus level, yet four, six and seven samples were able to capture 80% of the phylum-level, family-level, and genus-level diversity, respectively. This study for the first time reveals hyperlocal variations in riverine microbiomes and their assembly mechanisms, demanding attention to more robust sampling strategies for documenting microbial diversity in riverine systems.
|
Keywords
Microbiome
Freshwater
Taxon accumulation curve
Community assembly
|
Corresponding Author(s):
Fangqiong Ling
|
Issue Date: 16 May 2022
|
|
1 |
T J Battin, S Luyssaert, L A Kaplan, A K Aufdenkampe, A Richter, L J Tranvik. (2009). The boundless carbon cycle. Nature Geoscience, 2( 9): 598– 600
https://doi.org/10.1038/ngeo618
|
2 |
E Bolyen, J R Rideout, M R Dillon, N A Bokulich, C C Abnet, G A Al-Ghalith, H Alexander, E J Alm, M Arumugam, F Asnicar. et al.. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37( 8): 852– 857
https://doi.org/10.1038/s41587-019-0209-9
|
3 |
B J Callahan, P J McMurdie, M J Rosen, A W Han, A J A Johnson, S P Holmes. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13( 7): 581– 583
https://doi.org/10.1038/nmeth.3869
|
4 |
N W Charon, A Cockburn, C Li, J Liu, K A Miller, M R Miller, M A Motaleb, C W Wolgemuth. (2012). The unique paradigm of spirochete motility and chemotaxis. Annual Review of Microbiology, 66( 1): 349– 370
https://doi.org/10.1146/annurev-micro-092611-150145
|
5 |
J J Cole Y T Prairie N F Caraco W H McDowell L J Tranvik R G Striegl C M P Duarte J A Kortelainen J A Downing J J Middelburg J (2007) Melack. Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget. Ecosystems (New York, N.Y.), 10( 1): 172− 185
|
6 |
P Cruaud, A Vigneron, M S Fradette, C C Dorea, A I Culley, M J Rodriguez, S J Charette. (2020). Annual bacterial community cycle in a seasonally ice-covered river reflects environmental and climatic conditions. Limnology and Oceanography, 65( S1): S21– S37
https://doi.org/10.1002/lno.11130
|
7 |
B C Crump, L A Amaral-Zettler, G W Kling. (2012). Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME journal, 6( 9): 1629– 1639
https://doi.org/10.1038/ismej.2012.9
|
8 |
S H Ensign M W Doyle (2006). Nutrient spiraling in streams and river networks. Journal of Geophysical Research. Biogeosciences, 111(G4)
|
9 |
P G Falkowski, T Fenchel, E F Delong. (2008). The microbial engines that drive Earth’s biogeochemical cycles. Science, 320( 5879): 1034– 1039
https://doi.org/10.1126/science.1153213
|
10 |
C Fasching, C Akotoye, M Bižić, J Fonvielle, D Ionescu, S Mathavarajah, L Zoccarato, D A Walsh, H Grossart, M A Xenopoulos. (2020). Linking stream microbial community functional genes to dissolved organic matter and inorganic nutrients. Limnology and Oceanography, 65( S1): S71– S87
https://doi.org/10.1002/lno.11356
|
11 |
T Fukami ( 2015). Historical contingency in community assembly: Integrating niches, species pools, and priority effects. Annual Review of Ecology, Evolution, and Systematics, 46( 1): 1− 23
|
12 |
D J Gilvear M T Greenwood M C Thoms P J Wood ( 2016). River Science: Research and Management for the 21st Century. Hoboken: John Wiley & Sons
|
13 |
H S Gweon, M J Bowes, H L Moorhouse, A E Oliver, M J Bailey, M C Acreman, D S Read. (2021). Contrasting community assembly processes structure lotic bacteria metacommunities along the river continuum. Environmental Microbiology, 23( 1): 484– 498
https://doi.org/10.1111/1462-2920.15337
|
14 |
A Khleborodova ( 2020). Lefser: R implementation of the LEfSE method for microbiome biomarker discovery (Version R package version 140)
|
15 |
J Larsbrink, L S McKee. (2020). Bacteroidetes bacteria in the soil: Glycan acquisition, enzyme secretion, and gliding motility. Advances in Applied Microbiology, 110 : 63– 98
https://doi.org/10.1016/bs.aambs.2019.11.001
|
16 |
G E Leventhal, C Boix, U Kuechler, T N Enke, E Sliwerska, C Holliger, O X Cordero. (2018). Strain-level diversity drives alternative community types in millimetre-scale granular biofilms. Nature Microbiology, 3( 11): 1295– 1303
https://doi.org/10.1038/s41564-018-0242-3
|
17 |
F Ling, R Whitaker, M W LeChevallier, W T Liu. (2018). Drinking water microbiome assembly induced by water stagnation. The ISME journal, 12( 6): 1520– 1531
https://doi.org/10.1038/s41396-018-0101-5
|
18 |
S Louca, M F Polz, F Mazel, M B N Albright, J A Huber, M I O’Connor, M Ackermann, A S Hahn, D S Srivastava, S A Crowe, M Doebeli, L W Parfrey. (2018). Function and functional redundancy in microbial systems. Nature Ecology & Evolution, 2( 6): 936– 943
https://doi.org/10.1038/s41559-018-0519-1
|
19 |
S L McLellan, J C Fisher, R J Newton. (2015). The microbiome of urban waters. International microbiology: The official journal of the Spanish Society for Microbiology, 18( 3): 141– 149
|
20 |
P J McMurdie, S Holmes. (2013). Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8( 4): e61217
https://doi.org/10.1371/journal.pone.0061217
|
21 |
R J Newton, S E Jones, A Eiler, K D McMahon, S Bertilsson. (2011). A guide to the natural history of freshwater lake bacteria. Microbiology and molecular biology reviews, 75( 1): 14– 49
https://doi.org/10.1128/MMBR.00028-10
|
22 |
J Oksanen F G Blanchet R Kindt P Legendre P R Minchin R B O’Hara G L Simpson P Solymos M H H Stevens H Wagner ( 2020). Vegan: Community Ecology Package (Version R package version 25−7)
|
23 |
E Paradis J Claude K Strimmer ( 2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England), 20( 2): 289− 290
pmid: 14734327
|
24 |
S P Preheim, A R Perrotta, J Friedman, C Smilie, I Brito, M B Smith, E Alm. (2013). Computational methods for high-throughput comparative analyses of natural microbial communities. Methods in Enzymology, 531 : 353– 370
https://doi.org/10.1016/B978-0-12-407863-5.00018-6
|
25 |
C Quast E Pruesse P Yilmaz J Gerken T Schweer P Yarza J Peplies F O Glöckner ( 2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue): D590–D596
pmid: 23193283
|
26 |
D S Read, H S Gweon, M J Bowes, L K Newbold, D Field, M J Bailey, R I Griffiths. (2015). Catchment-scale biogeography of riverine bacterioplankton. ISME journal, 9( 2): 516– 526
https://doi.org/10.1038/ismej.2014.166
|
27 |
C Ruiz-González, J P Niño-García, Giorgio P A Del. (2015). Terrestrial origin of bacterial communities in complex boreal freshwater networks. Ecology Letters, 18( 11): 1198– 1206
https://doi.org/10.1111/ele.12499
|
28 |
D Savio, L Sinclair, U Z Ijaz, J Parajka, G H Reischer, P Stadler, A P Blaschke, G Blöschl, R L Mach, A K T Kirschner, A H Farnleitner, A Eiler. (2015). Bacterial diversity along a 2600 km river continuum. Environmental Microbiology, 17( 12): 4994– 5007
https://doi.org/10.1111/1462-2920.12886
|
29 |
N Segata, J Izard, L Waldron, D Gevers, L Miropolsky, W S Garrett, C Huttenhower. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12( 6): R60
https://doi.org/10.1186/gb-2011-12-6-r60
|
30 |
P Svoboda, E S Lindström, Osman O Ahmed, S Langenheder. (2018). Dispersal timing determines the importance of priority effects in bacterial communities. ISME journal, 12( 2): 644– 646
https://doi.org/10.1038/ismej.2017.180
|
31 |
Missouri Department of Natural Resources (2015) The. The state of our Missouri waters-Meramec river watershed. Retrieved from www.ewgatewayorg/wp-content/uploads/ 2017.08/MRP-MeramecRiverWatershed.pdf
|
32 |
J R Thompson, S Pacocha, C Pharino, V Klepac-Ceraj, D E Hunt, J Benoit, R Sarma-Rupavtarm, D L Distel, M F Polz. (2005). Genotypic diversity within a natural coastal bacterioplankton population. Science, 307( 5713): 1311– 1313
https://doi.org/10.1126/science.1106028
|
33 |
R L Vannote, G W Minshall, K W Cummins, J R Sedell, C E Cushing. (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, 37( 1): 130– 137
https://doi.org/10.1139/f80-017
|
34 |
H Wickham, M Averick, J Bryan, W Chang, L McGowan, R François, G Grolemund, A Hayes, L Henry, J Hester. et al.. (2019). Welcome to the Tidyverse. Journal of Open Source Software, 4( 43): 1686
https://doi.org/10.21105/joss.01686
|
35 |
P J A Withers, H P Jarvie. (2008). Delivery and cycling of phosphorus in rivers: A review. Science of the total environment, 400( 1−3): 379– 395
https://doi.org/10.1016/j.scitotenv.2008.08.002
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|