Tidal levels significantly change bacterial community composition in a tropical estuary during the dry season

Abstract

Estuaries are usually characterized by strong spatial and temporal variability in water physicochemical conditions and are often largely affected by human activities. One important source of variability is caused by tides that can swiftly alter not only physicochemical conditions but also the abundance and composition of the biota. The effect of the diurnal tidal cycle on microbial community composition during different seasons remains uncertain, although this knowledge underlies having effective monitoring programs for water quality and potential identification of health risk conditions. In this study, we assessed the bacterioplankton community composition and diversity across four tidal water levels in a tropical estuary characterized by a mixed semidiurnal tide regime (i.e., two high and two low tides of varying amplitudes) during both dry and wet seasons. The bacterial community composition varied significantly among the four tidal levels, but only during the dry season, when the influence of the seawater intrusion was largest. Bacterial indicators’ taxa identified using the Indicator Value Index were found within Cyanobacteria, Actinobacteriota, Bacteroidota, and Proteobacteria. The indicator taxon Cyanobium sp. had a prominent presence across multiple tidal levels. The main predicted phenotypes of the bacterial communities were associated with potential pathogenicity, gram-negative, and biofilm formation traits. While there were no marked predicted phenotypic differences between seasons, pathogenic and gram-negative traits were more prevalent in the dry season, while biofilm formation traits dominated in the wet season. Overall, our findings underscore the intricate relationship between river hydrodynamics and bacterial composition variability and hint a significant human impact on the water quality of the Bangpakong River.

Keywords

Rivers / Brackish systems / Tides / Bacterial indicators / Water pollution

References

[1] Alonso C, Pereira E, Bertoglio F, De Cáceres M, Amann R. Bacterioplankton composition as an indicator of environmental status: proof of principle using indicator value analysis of estuarine communities. Aquat Microb Ecol. 2022, 88: 1-18

[2] Astudillo-García C, Hermans SM, Stevenson B, Buckley H, Lear G. Microbial assemblages and bioindicators as proxies for ecosystem health status: potential and limitations. Appl Microbiol Biotechnol. 2019, 103: 6407-6421

[3] Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier C, Silliman R. The value of estuarine and coastal ecosystem services. Ecol Monogr. 2011, 81: 169-193

[4] Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packmann A. The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol. 2016, 14: 251-263

[5] Begmatov S, Savvichev AS, Kadnikov VV, Beletsky AV, Rusanov II, Klyuvitkin AA, Novichkova EA, Mardanov AV, Pimenov NV, Ravin NV. Microbial communities involved in methane, sulfur, and nitrogen cycling in the sediments of the Barents sea. Microorganisms. 2021, 9: 2362

[6] Boonphakdee T, Sawangwong P, Fujiwara T. Freshwater discharge of Bangpakong River flowing into the inner Gulf of Thailand. La Mer. 1999, 37: 103-109

[7] Boonphakdee T, Kasai A, Fujiwara T, Sawangwong P, Cheevaporn V. Combined stable carbon isotope and c/n ratios as indicators of source and fate of organic matter in the Bangpakong River Estuary, Thailand. EnvironmentAsia. 2008, 1: 28-36

[8] Bordalo AA, Nilsumranchit W, Chalermwat K. Water quality and uses of the Bangpakong River (eastern Thailand). Water Res. 2001, 35: 3635-3642

[9] Bordalo AA, Chalermwat K, Teixeira C. Nutrient variability and its influence on nitrogen processes in a highly turbid tropical estuary (Bangpakong, Gulf of Thailand). J Environ Sci. 2016, 45: 131-142

[10] Bouvier TC, del Giorgio PA. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr. 2002, 47: 453-470

[11] Bundao S, Veeravaitaya N, Kaewnern M, Ingthamjitr S. The relationship between land use and water quality in Bangpakong Estuary, Thailand. J Fish Environ. 2018, 42: 24-31

[12] Cáceres M, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009, 90: 3566-3574

[13] Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson A, Holmes S. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016, 13: 581-583

[14] Camberg JL, Sandkvist M. Molecular analysis of the Vibrio cholerae type II secretion ATPase EpsE. J Bacteriol. 2005, 187: 249-256

[15] Campbell BJ, Kirchman DL. Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J. 2013, 7: 210-220

[16] Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Nat Acad Sci. 2011, 108: 4516-4522

[17] Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J. Correction to: Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome. 2019, 7: 148

[18] Chen X, Wei W, Wang J, Li H, Sun J, Ma R, Jiao N, Zhang R. Tide driven microbial dynamics through virus-host interactions in the estuarine ecosystem. Water Res. 2019, 160: 118-129

[19] Clark DR, McKew BA, Binley A, Heppell C, Whitby C, Trimmer M. Hydrological properties predict the composition of microbial communities cycling methane and nitrogen in rivers. ISME Commun. 2022, 2: 5

[20] Costa MS, Costa M, Ramos V, Leao PN, Barreiro A, Vasconcelos V, Martins R. Picocyanobacteria from a clade of marine Cyanobium revealed bioactive potential against microalgae, bacteria, and marine invertebrates. J Toxicol Environ Health Part A. 2015, 78: 432-442

[21] Crump BC, Hopkinson CS, Sogin ML, Hobbie JE. Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol. 2004, 70: 1494-1505

[22] Day JW, Crump BC, Kemp WM, Yáñez-Arancibia A. Estuarine ecology. 2012, Hoboken, Wiley

[23] De Boer PL, Oost AP, Vi MJ. The diurnal inequality of the tide as a parameter for recognizing tidal influences. Sepm Jsr. 1989, 59: 912-921

[24] DeLorenzo S, Bräuer SL, Edgmont CA, Herfort L, Tebo BM, Zuber P. Ubiquitous dissolved inorganic carbon assimilation by marine bacteria in the Pacific Northwest coastal ocean as determined by stable isotope probing. PLoS ONE. 2012, 7 e46695

[25] Diner RE, Zimmer-Faust A, Cooksey E, Allard S, Kodera SM, Kunselman E, Garodia Y, Verhougstraete MP, Allen AE, Griffith J, Gilbert J. Host and water microbiota are differentially linked to potential human pathogen accumulation in oysters. Appl Environ Microbiol. 2023, 89 e0031823

[26] Elliott M, McLusky DS. The need for definitions in understanding estuaries. Estuar Coast Shelf Sci. 2002, 55: 815-827

[27] Ensign SH, Doyle MW, Piehler MF. The effect of tide on the hydrology and morphology of a freshwater river. Earth Surf Process Landforms. 2013, 38: 655-660

[28] Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992, 61: 1-10

[29] Findlay S. Stream microbial ecology. J N Am Benthol Soc. 2010, 29: 170-181

[30] Fine PV, Kembel SW. Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography. 2011, 34: 552-565

[31] Garrido-Oter R, Nakano RT, Dombrowski N, Ma KW, Agbiome MAC, Schulze-Lefert P. Modular traits of the rhizobiales root microbiota and their evolutionary relationship with Symbiotic Rhizobia. Cell Host Microbe. 2018, 24: 155-167

[32] Ghosh A, Bhadury P. Exploring biogeographic patterns of bacterioplankton communities across global estuaries. Microbiologyopen. 2019, 8 e00741

[33] Gong F, Huang S, Xie W, Zhang H, Lan F, Yin K. Effects of tidal cycles on the variability of microbial communities in a semiclosed bay. Cont Shelf Res. 2024, 272 105147

[34] Graham ED, Tully BJ. Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. ISME J. 2021, 15: 1248-1256

[35] Guizien K, Dupuy C, Ory P, Montanie H, Hartmann H, Chatelain M, Karpyychev M. Microorganism dynamics during a rising tide: disentangling effects of resuspension and mixing with offshore waters above an intertidal mudflat. J Mar Syst. 2014, 129: 178-188

[36] Gupta RS. Microbial taxonomy: how and why name changes occur and their significance for (clinical) microbiology. Clin Chem. 2021, 68: 134-137

[37] Gutiérrez-Barral A, Teira E, Hernández-Ruiz M, Fernandez E. Response of prokaryote community composition to riverine and atmospheric nutrients in a coastal embayment: role of organic matter on Vibrionales. Estuar Coast Shelf Sci. 2021, 251 107196

[38] Herlemann D, Labrenz M, Jürgens K, Bertilsson S, Waniek J, Andersson A. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011, 5: 1571-1579

[39] Hoitink AJF, Jay DA. Tidal river dynamics: implications for deltas. Rev Geophys. 2016, 54: 240-272

[40] Jovanovic D, Coleman R, Deletic A, Maccarthy D. Tidal fluctuations influence E. coli concentrations in urban estuaries. Mar Pollut Bull. 2017, 119: 226-230

[41] Kieft B, Li Z, Bryson S, Crump B, Hettich R, Pan C, Mayali X, Mueller R. Microbial community structure-function relationships in Yaquina Bay estuary reveal spatially distinct carbon and nitrogen cycling capacities. Front Microbiol. 2018, 9: 1282

[42] Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega TRL, Knight R, Beiko RG, Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013, 31: 814-821

[43] Lee M, Park BS, Baek SH. Tidal influences on biotic and abiotic factors in the Seomjin River Estuary and Gwangyang Bay, Korea. Estuar Coast. 2018, 41: 1-17

[44] Liu J, Luo Y, Xu Z, Kjellerup B. Galanakis CM. Food pathogens. Innovative food analysis. 2021Elsevier: 295321

[45] Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15: 550

[46] Ma Y, Chanpiwat P. A case study on the correlation between land use types and water quality of the Bang Pakong River in Chachoengsao Province. Highl Sci Eng Technol. 2022, 20: 102-108

[47] Marín-Vindas C, Sebastián M, Ruiz-González C, Balague V, Vega-Corrales L, Gasol JM. Shifts in bacterioplankton community structure between dry and wet seasons in a tropical estuary strongly affected by riverine discharge. Sci Total Environ. 2023, 903: 166104

[48] Markowitz VM, Chen I-MA, Palaniappan K, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang J, Woyke T, Huntemann M, Anderson I, Billis K, Varghese N, Mavromatis K, Pati A, Ivanova NN, Kyrpides N. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 2014, 42: D560-D567

[49] Marshall IPG, Starnawski P, Cupit C, Fernandez-Caceres E, Ettema T, Schramm A, Kjeldsen KU. The novel bacterial phylum Calditrichaeota is diverse, widespread and abundant in marine sediments and has the capacity to degrade detrital proteins. Environ Microbiol Rep. 2017, 9: 397-403

[50] Matheus-Carnevali PB, Schulz F, Castelle CJ, Kantor RS, Shih PM, Sharon I, Santini JM, Olm MR, Amano Y, Thomas BC, Anantharaman K, Burstein D, Becraft ED, Stepanauskas R, Woyke T, Banfield J. Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria. Nat Commun. 2019, 10: 463

[51] McLellan SL, Eren AM. Discovering new indicators of fecal pollution. Trends Microbiol. 2014, 22: 697-706

[52] McLusky DS. Marine and estuarine gradients—an overview. Neth J Aquat Ecol. 1993, 27: 489-493

[53] Moftakhari HR, Jay DA, Talke SA, Kukulka T, Bromirski PD. A novel approach to flow estimation in tidal rivers. Water Resour Res. 2013, 49: 4817-4832

[54] Mou X, Sun S, Edwards RA, Hodson R, Moran MA. Bacterial carbon processing by generalist species in the coastal ocean. Nature. 2008, 451: 708-711

[55] Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 2018, 6: 140

[56] Murray KS, Fisher LE, Therrien J, George B, Gillespie J. Assessment and use of indicator bacteria to determine sources of pollution to an urban river. J Great Lakes Res. 2001, 27: 220-229

[57] O’Connor JA, Erler DV, Ferguson A, Maher DT. The tidal freshwater river zone: Physical properties and biogeochemical contribution to estuarine hypoxia and acidification—the “hydrologic switch”. Estuar Coast Shelf Sci. 2022, 268 107786

[58] Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, Ohara RB, Solymos P, Stevens MHH, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Antoniazi HB et al (2019) Vegan: Community Ecology Package., R Package Version 2.0-7. https://cran.r-project.org/web/packages/vegan/index.html. Accessed 29 Apr 2019

[59] Okwala T, Shrestha S, Ghimire S, Mohanasundaram S, Datta A. Assessment of climate change impacts on water balance and hydrological extremes in Bang Pakong-Prachin Buri river basin, Thailand. Environ Res. 2020, 186 109544

[60] Popoff MR, Bouvet P. Genetic characteristics of toxigenic Clostridia and toxin gene evolution. Toxicon. 2013, 75: 63-89

[61] Pusch M, Fiebig D, Brettar I, Eisenmann H, Ellis BK, Kaplan LA, Lock MA, Naegeli MW, Traunspurger W. The role of micro-organisms in the ecological connectivity of running waters. Freshw Biol. 1998, 40: 453-495

[62] Raymond PA, Hartmann J, Lauerwald R, Sobek S, McDonald C, Hoover M, Butman D, Striegl R, Mayorga E, Humborg C, Kortelainen P, Durr H, Meybeck M, Ciais P, Guth P. Global carbon dioxide emissions from inland waters. Nature. 2013, 503: 355-359

[63] Ruiz-González C, Niño-García JP, Del Giorgio PA. Terrestrial origin of bacterial communities in complex boreal freshwater networks. Ecol Lett. 2015, 18: 1198-1206

[64] Sangmanee C, Wattayakorn G, Sojisuporn P. Simulating changes in discharge and suspended sediment loads of the. Maejo Int J Sci Technol. 2013, 7: 72-84

[65] Sassi MG, Hoitink AJF. River flow controls on tides and tide-mean water level profiles in a tidal freshwater river. J Geophys Res Oceans. 2013, 118: 4139-4151

[66] Savio D, Sinclair L, Ijaz UZ, Parajka J, Reischer GH, Stadler P, Blaschke AP, Blöschl G, Mach RL, Kirschner AK, Farnleitner AH. Bacterial diversity along a 2600 km river continuum. Environ Microbiol. 2015, 17: 4994-5007

[67] Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garret W, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12: R60

[68] Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, Tandeau de Marsac N, Rippka R, Herdman M, Sivonen CT, Laurent T, Goodwin L, Nolan M, Davenport KW, Han CS, Rubin EM, Eisen JA, et al. . Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA. 2013, 110: 1053-1058

[69] Silva CSP, Genuário DB, Vaz MG, Fiore MF. Phylogeny of culturable cyanobacteria from Brazilian mangroves. Syst Appl Microbiol. 2014, 37: 100-112

[70] Sipler RE, Kellogg CTE, Connelly TL, Roberts QN, Yager PL, Bronk DA. Microbial community response to terrestrially derived dissolved organic matter in the coastal arctic. Front Microbiol. 2017, 8: 1018

[71] Snyder EE, Kampanya N, Lu J, Nordberg EK, Karur HR, Shukla M, Soneja J, Xue T, Yoo H, Zhang F, Dharmanolla C, Dongre NV, Gillespie JJ, Hamelius J, Hance M, Huntington KI, Jukneliene D, Koziski J, Mackasmiel L, Mane SP. PATRIC: the VBI pathosystems resource integration center. Nucleic Acids Res. 2007, 35: D401-D406

[72] Spietz RL, Williams CM, Rocap G, Horner-Devine MC. A dissolved oxygen threshold for shifts in bacterial community structure in a seasonally hypoxic estuary. PLoS ONE. 2015, 10 e0135731

[73] Swinbanks DD. Intertidal exposure zones: a way to subdivide the shore. J Exp Mar Biol Ecol. 1982, 62: 69-86

[74] Tao W, Niu L, Liu F, Cai H, Ou S, Zeng D, Lou Q, Yang Q. Influence of river-tide dynamics on phytoplankton variability and their ecological implications in two Chinese tropical estuaries. Ecol Ind. 2020, 115 106458

[75] URycki DR, Good SP, Crump BC, Chadwick J, Jones GD. River microbiome composition reflects macroscale climatic and geomorphic differences in headwater streams. Front Water. 2020, 2: 574728

[76] van der Stel A-X, Wösten MMSM. Regulation of respiratory pathways in campylobacterota: a review. Front Microbiol. 2019, 10: 1719

[77] Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D, Spear JR, Caporaso G, Blekhman R, Knight R, Fink R, Knights D (2017) Bugbase predicts organism level microbiome phenotypes. BioRxiv

[78] Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R, Ragan MA, Schmidt S, Hugenholtz, . Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat Commun. 2017, 8: 215

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