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Untapped rich microbiota of mangroves of Pakistan: diversity and community compositions

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Abstract

The mangrove ecosystem is the world’s fourth most productive ecosystem in terms of service value and offering rich biological resources. Microorganisms play vital roles in these ecological processes, thus researching the mangroves-microbiota is crucial for a deeper comprehension of mangroves dynamics. Amplicon sequencing that targeted V4 region of 16S rRNA gene was employed to profile the microbial diversities and community compositions of 19 soil samples, which were collected from the rhizosphere of 3 plant species (i.e., Avicennia marina, Ceriops tagal, and Rhizophora mucronata) in the mangrove forests of Lasbela coast, Pakistan. A total of 67 bacterial phyla were observed from three mangroves species, and these taxa were classified into 188 classes, 453 orders, 759 families, and 1327 genera. We found that Proteobacteria (34.9–38.4%) and Desulfobacteria (7.6–10.0%) were the dominant phyla followed by Chloroflexi (6.6–7.3%), Gemmatimonadota (5.4–6.8%), Bacteroidota (4.3–5.5%), Planctomycetota (4.4–4.9%) and Acidobacteriota (2.7–3.4%), Actinobacteriota (2.5–3.3%), and Crenarchaeota (2.5–3.3%). After considering the distribution of taxonomic groups, we prescribe that the distinctions in bacterial community composition and diversity are ascribed to the changes in physicochemical attributes of the soil samples (i.e., electrical conductivity (ECe), pH, total organic matter (OM), total organic carbon (OC), available phosphorus (P), and extractable potassium (CaCO3). The findings of this study indicated a high-level species diversity in Pakistani mangroves. The outcomes may also aid in the development of effective conservation policies for mangrove ecosystems, which have been hotspots for anthropogenic impacts in Pakistan. To our knowledge, this is the first microbial research from a Pakistani mangrove forest.

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Data availability

The collected reads were deposited in GenBank under Bio Project accession number PRJNA817083 and BioSample accession numbers SAMN26747204–SAMN26747222 (in total 19 samples).

References

  • Alongi DM (2012) Carbon sequestration in mangrove forests. Carbon Manag 3:313–322

    Article  CAS  Google Scholar 

  • Alongi DM (2020) Nitrogen cycling and mass balance in the world’s mangrove forests. Nitrogen 1:167–189

    Article  Google Scholar 

  • Ananda K, Sridhar K (2002) Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. Can J Microbiol 48:871–878

    Article  CAS  PubMed  Google Scholar 

  • Andreote FD, Jimenez DJ, Chaves D, Dias AC, Luvizotto DM, Dini-Andreote F, Fasanella CC, Lopez MV, Baena S, Taketani RG, de Melo IS (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS ONE 7:e38600. https://doi.org/10.1371/journal.pone.0038600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aziz I, Khan MA (2000) Physiological adaptations of Avicennia marina to seawater concentrations in the indus delta, Pakistan. Pak J Bot 32:151–169

    Google Scholar 

  • Azman AS, Othman I, Velu SS, Chan KG, Lee LH (2015) Mangrove rare actinobacteria: taxonomy, natural compound, and discovery of bioactivity. Front Microbiol 6:856. https://doi.org/10.3389/fmicb.2015.00856

    Article  PubMed  PubMed Central  Google Scholar 

  • Balk M, Keuskamp JA, Laanbroek HJ (2016) Potential for sulfate reduction in mangrove forest soils: comparison between two dominant species of the Americas. Front Microbiol 7:1855. https://doi.org/10.3389/fmicb.2016.01855

    Article  PubMed  PubMed Central  Google Scholar 

  • Basak P, Pramanik A, Roy R, Chattopadhyay D, Bhattacharyya M (2015) Cataloguing the bacterial diversity of the Sundarbans mangrove, India in the light of metagenomics. Genom Data 4:90–92. https://doi.org/10.1016/j.gdata.2015.03.014

    Article  PubMed  PubMed Central  Google Scholar 

  • Basyuni M, Slamet B, Sulistiyono N, Munir E, Vovides A, Bunting P (2021) Physicochemical characteristics, nutrients, and fish production in different types of mangrove forests in North Sumatra and the Aceh Provinces of Indonesia. Kuwait J Sci 48

  • Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc Nat Acad Sci 108:19473–19481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci 105:10583–10588. https://doi.org/10.1073/pnas.0709942105

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolyen 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-Rodriguez 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, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukin YS, Galachyants YP, Morozov I, Bukin S, Zakharenko A, Zemskaya T (2019) The effect of 16S rRNA region choice on bacterial community metabarcoding results. Sci Data 6:1–14

    Article  Google Scholar 

  • Cabral L, Júnior GVL, de Sousa STP, Dias ACF, Cadete LL, Andreote FD, Hess M, de Oliveira VM (2016) Anthropogenic impact on mangrove sediments triggers differential responses in the heavy metals and antibiotic resistomes of microbial communities. Environ Pollut 216:460–469

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522. https://doi.org/10.1073/pnas.1000080107

    Article  PubMed  Google Scholar 

  • Carlson RR, Evans LJ, Foo SA, Grady BW, Li J, Seeley M, Xu Y, Asner GP (2021) Synergistic benefits of conserving land-sea ecosystems. Glob Ecol Conserv 28:e01684

    Article  Google Scholar 

  • Curtis TP, Sloan WT (2004) Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol 7:221–226. https://doi.org/10.1016/j.mib.2004.04.010

    Article  PubMed  Google Scholar 

  • Das S, De M, Ganguly D, Maiti TK, Mukherjee A, Jana TK, De TK (2012) Depth integrated microbial community and physico-chemical properties in mangrove soil of Sundarban. India Adv Microbiol 2:234

    Article  Google Scholar 

  • Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Sci 359:320–325

    Article  CAS  Google Scholar 

  • Díez-Vives C, Gasol JM, Acinas SG (2014) Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea. Syst Appl Microbiol 37:68–78

    Article  PubMed  Google Scholar 

  • dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS ONE 6:e16943. https://doi.org/10.1371/journal.pone.0016943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubey A, Malla MA, Khan F, Chowdhary K, Yadav S, Kumar A, Sharma S, Khare PK, Khan ML (2019) Soil microbiome: a key player for conservation of soil health under changing climate. Biodivers Conserv 28:2405–2429

    Article  Google Scholar 

  • Edgar CR (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–1001. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  • Fadeev E, Cardozo-Mino MG, Rapp JZ, Bienhold C, Salter I, Salman-Carvalho V, Molari M, Tegetmeyer HE, Buttigieg PL, Boetius A (2021) Comparison of two 16S rRNA primers (V3–V4 and V4–V5) for studies of arctic microbial communities. Front Microbiol 12:637526

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandes SO, Kirchman DL, Michotey VD, Bonin PC, LokaBharathi PA (2014) Bacterial diversity in relatively pristine and anthropogenically-influenced mangrove ecosystems (Goa, India). Braz J Microbiol 45:1161–1171. https://doi.org/10.1590/s1517-83822014000400006

    Article  CAS  PubMed  Google Scholar 

  • Foesel BU, Rohde M, Overmann J (2013) Blastocatella fastidiosa gen. nov., sp. nov., isolated from semiarid savanna soil - the first described species of Acidobacteria subdivision 4. Syst Appl Microbiol 36:82–89. https://doi.org/10.1016/j.syapm.2012.11.002

    Article  CAS  PubMed  Google Scholar 

  • Fortunato CS, Crump BC (2015) Microbial gene abundance and expression patterns across a river to ocean salinity gradient. PLoS ONE 10:e0140578

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghizelini AM, Mendonça-Hagler LCS, Macrae A (2012) Microbial diversity in Brazilian mangrove sediments: a mini review. Brazil J Microbiol 43:1242–1254

    Article  Google Scholar 

  • Ghosh A, Bhadury P (2018) Investigating monsoon and post-monsoon variabilities of bacterioplankton communities in a mangrove ecosystem. Environ Sci Pollut Res 25:5722–5739

    Article  CAS  Google Scholar 

  • Ghosh A, Dey N, Bera A, Tiwari A, Sathyaniranjan KB, Chakrabarti K, Chattopadhyay D (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarban. India Saline Syst 6:1. https://doi.org/10.1186/1746-1448-6-1

    Article  CAS  PubMed  Google Scholar 

  • Gilbert JA, Meyer F, Bailey MJ (2011) The future of microbial metagenomics (or is ignorance bliss?). ISME J 5:777–779

    Article  PubMed  Google Scholar 

  • Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2011) Status and distribution of mangrove forests of the world using earth observation satellite data. Glob Ecol Biogeogr 20:154–159. https://doi.org/10.1111/j.1466-8238.2010.00584

    Article  Google Scholar 

  • Gomes NC, Flocco CG, Costa R, Junca H, Vilchez R, Pieper DH, Krogerrecklenfort E, Paranhos R, Mendonca-Hagler LC, Smalla K (2010) Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Microbiol Ecol 74:276–290. https://doi.org/10.1111/j.1574-6941.2010.00962.x

    Article  CAS  PubMed  Google Scholar 

  • Gotelli NJ, Chao A (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In: Levin SA (ed) Encyclopedia of Biodiversity, 2nd edn. Academic Press, Waltham, pp 195–211

    Chapter  Google Scholar 

  • Haldar S, Nazareth SW (2018) Taxonomic diversity of bacteria from mangrove sediments of Goa: metagenomic and functional analysis. 3 Biotech 8:1–10

  • Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hewson I, Steele JA, Capone DG, Fuhrman JA (2006) Remarkable heterogeneity in meso-and bathypelagic bacterioplankton assemblage composition. Limnol Oceanogr 51:1274–1283

    Article  Google Scholar 

  • Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fert Soils 33:265–278. https://doi.org/10.1007/s003740000319

    Article  CAS  Google Scholar 

  • Hong Y, Liao D, Hu A, Wang H, Chen J, Khan S, Su J, Li H (2015) Diversity of endophytic and rhizoplane bacterial communities associated with exotic Spartina alterniflora and native mangrove using Illumina amplicon sequencing. Canad J Microbiol 61:723–733

    Article  CAS  Google Scholar 

  • Hou L, Zheng Y, Liu M, Gong J, Zhang X, Yin G, You L (2013) Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze Estuary. J Geophys Res Biogeosci 118:1237–1246

    Article  CAS  Google Scholar 

  • Hu C, Cao Z (2007) Size and activity of the soil microbial biomass and soil enzyme activity in long-term field experiments. World J Agr Sci 3:63–70

    Google Scholar 

  • Imchen M, Kumavath R, Barh D, Vaz A, Góes-Neto A, Tiwari S, Ghosh P, Wattam AR, Azevedo V (2018) Comparative mangrove metagenome reveals global prevalence of heavy metals and antibiotic resistome across different ecosystems. Sci Rep 8:1–15

    Article  Google Scholar 

  • Jansson JK, Hofmockel KS (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18:35–46

    Article  CAS  PubMed  Google Scholar 

  • Jiang XT, Peng X, Deng GH, Sheng HF, Wang Y, Zhou HW, Tam NF (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104. https://doi.org/10.1007/s00248-013-0238-8

    Article  PubMed  Google Scholar 

  • Joshi H, Ghose M (2003) Forest structure and species distribution along soil salinity and pH gradient in mangrove swamps of the Sundarbans. Trop Ecol 44:195–204

    Google Scholar 

  • Kannan S, Balamurugan S, Ragavan P, Deivasigamani B, Wee A, Salmo S, Basyuni M, Kajita T (2022) eDNA envisaged conservation of IUCN threatened taxa of the tropical mangrove ecosystems. IOP Conf Ser Earth Environ Sci 1115:012032 (IOP Publishing)

    Article  Google Scholar 

  • Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Adv Mar Biol 40:81–251. https://doi.org/10.1016/S0065-2881(01)40003-4

    Article  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. The prokaryotes: a handbook on the biology of bacteria. Springer, pp 3–37

    Chapter  Google Scholar 

  • Kim M, Morrison M, Yu Z (2011) Evaluation of different partial 16S rRNA gene sequence regions for phylogenetic analysis of microbiomes. J Microbiol Methods 84:81–87

    Article  CAS  PubMed  Google Scholar 

  • Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50:1697–1706

    Article  CAS  Google Scholar 

  • Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Microbiol 27:1E.5.1–1E.5.20

  • Li M, Cao H, Hong Y, Gu JD (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243–1254. https://doi.org/10.1007/s00253-010-2929-0

    Article  CAS  PubMed  Google Scholar 

  • Liang J-B, Chen Y-Q, Lan C-Y, Tam NFY, Zan Q-J, Huang L-N (2006) Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 739–747. https://doi.org/10.1007/s00227-006-0377-2

  • Liao P-C, Huang B-H, Huang S (2007) Microbial community composition of the Danshui river estuary of Northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microbial Ecol 54:497–507

    Article  Google Scholar 

  • Liao S, Wang Y, Liu H, Fan G, Sahu SK, Jin T, Chen J, Zhang P, Gram L, Strube ML (2020) Deciphering the microbial taxonomy and functionality of two diverse mangrove ecosystems and their potential abilities to produce bioactive compounds. Msystems 5:e00851-e1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Huang H, Bao S, Tong Y (2019) Microbial community structure of soils in Bamenwan mangrove wetland. Sci Rep 9:8406. https://doi.org/10.1038/s41598-019-44788-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru AE, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100. https://doi.org/10.1016/B978-0-12-387661-4.00004-5

    Article  CAS  PubMed  Google Scholar 

  • Lyimo TJ, Pol A, Harhangi HR, Jetten MS, Op den Camp HJ (2009) Anaerobic oxidation of dimethylsulfide and methanethiol in mangrove sediments is dominated by sulfate-reducing bacteria. FEMS Microbiol Ecol 70:483–492

    Article  CAS  PubMed  Google Scholar 

  • Lyimo TJ, Pol A, den Camp HJO (2002) Sulfate reduction and methanogenesis in sediments of Mtoni mangrove forest, Tanzania. AMBIO J Hum Environ 31:614–616

    Article  Google Scholar 

  • Menéndez P, Losada IJ, Torres-Ortega S, Narayan S, Beck MW (2020) The global flood protection benefits of mangroves. Sci Rep 10:4404. https://doi.org/10.1038/s41598-020-61136-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller RO, Gavlak R, Horneck D (2013) Soil, plant and water reference methods for the western region. Fort Collins, CO, USA, Colorado State University

    Google Scholar 

  • Mujakić I, Piwosz K, Koblížek M (2022) Phylum Gemmatimonadota and its role in the environment. Microorganisms 10:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen LD, Nguyen CT, Le HS, Tran BQ (2019) Mangrove mapping and above-ground biomass change detection using satellite images in coastal areas of Thai Binh Province. Vietnam for Soc 3:248–261

    Google Scholar 

  • Nogales B, Aguiló-Ferretjans MM, Martín-Cardona C, Lalucat J, Bosch R (2007) Bacterial diversity, composition and dynamics in and around recreational coastal areas. Environ Microbiol 9:1913–1929

    Article  CAS  PubMed  Google Scholar 

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture

    Google Scholar 

  • 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. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023

    Article  CAS  PubMed  Google Scholar 

  • Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinform 26:715–721

    Article  CAS  Google Scholar 

  • Peixoto R, Chaer GM, Carmo FL, Araujo FV, Paes JE, Volpon A, Santiago GA, Rosado AS (2011) Bacterial communities reflect the spatial variation in pollutant levels in Brazilian mangrove sediment. Anton Leeuw Int J G 99:341–354. https://doi.org/10.1007/s10482-010-9499-0

    Article  CAS  Google Scholar 

  • Perera K, Amarasinghe M, Somaratna S (2013) Vegetation structure and species distribution of mangroves along a soil salinity gradient in a micro tidal estuary on the north-western coast of Sri Lanka. American J Mar Sci 7–15

  • Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrasé C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu W, Lin D, Zhang Z, Di W, Gao B, Zeng R (2018) Metagenomics investigation of agarlytic genes and genomes in mangrove sediments in China: a potential repertory for carbohydrate-active enzymes. Front Microbiol 9:1864. https://doi.org/10.3389/fmicb.2018.01864

    Article  PubMed  PubMed Central  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rampadarath S, Bandhoa K, Puchooa D, Jeewon R, Bal S (2018) Metatranscriptomics analysis of mangroves habitats around Mauritius. World J Microbiol Biotechnol 34:59. https://doi.org/10.1007/s11274-018-2442-7

    Article  PubMed  Google Scholar 

  • Rasool F, Tunio S, Hasnain S, Ahmad E (2002) Mangrove conservation along the coast of Sonmiani, Balochistan, Pakistan. Trees 16:213–217

    Article  Google Scholar 

  • Reyes R, Fortes M (1985) Litter production and leaf litter decomposition rates of mangrove trees in Pagbilao, Quezon. Report on microbial aspects of nutrient cycling in mangrove environments, UNDP/UNESCO (RAS/79/002). Philippines, Manila, pp 72–73

    Google Scholar 

  • Richards L (1954) Diagnosis and improvement of saline and alkali soils (USDA). Handbook. 60. US. Govt., Printing Office, Washington

  • Rishan ST, Kline RJ, Rahman MS (2023) Applications of environmental DNA (eDNA) to detect subterranean and aquatic invasive species: a critical review on the challenges and limitations of eDNA metabarcoding. Environ Adv 100370

  • Rivas-Marin E, Canosa I, Devos DP (2016) Evolutionary cell biology of division mode in the bacterial Planctomycetes-Verrucomicrobia- Chlamydiae Superphylum. Front Microbiol 7:1964. https://doi.org/10.3389/fmicb.2016.01964

    Article  PubMed  PubMed Central  Google Scholar 

  • Rocha LL, Colares GB, Nogueira VL, Paes FA, Melo VM (2016) Distinct habitats select particular bacterial communities in mangrove sediments. Int J Microbiol 2016:3435809. https://doi.org/10.1155/2016/3435809

    Article  PubMed  PubMed Central  Google Scholar 

  • Roger AJ, Munoz-Gomez SA, Kamikawa R (2017) The origin and diversification of mitochondria. Curr Biol 27:R1177–R1192. https://doi.org/10.1016/j.cub.2017.09.015

    Article  CAS  PubMed  Google Scholar 

  • Rong X, Zhang W, Xu B, Li P, Wu H, Jin Y, Wang R (2020) Comparative analysis of bacterial community diversity between soil and water of Dongzhai Harbor Mangrove reserve using 16S rRNA gene sequencing and shotgun metagenomic sequencing. Res Sq (Preprint). https://doi.org/10.21203/rs.3.rs-114741/v1

  • Saifullah S, Rasool F (2002) Mangroves of Miani Hor lagoon on the north Arabian Sea coast of Pakistan. Pak J Bot 34:303–310

    Google Scholar 

  • Saunders D, Kalff J (2001) Denitrification rates in the sediments of Lake Memphremagog, Canada–USA. Water Res 35:1897–1904. https://doi.org/10.1016/S0043-1354(00)00479-6

    Article  CAS  PubMed  Google Scholar 

  • Schlaeppi K, Ronchi F, Leib SL, Erb M, Ramette A (2020) Evaluation of primer pairs for microbiome profiling from soils to humans within the One Health framework. Mol Ecol Resour 20:1558–1571

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Handelsman J (2008) A statistical toolbox for metagenomics: assessing functional diversity in microbial communities. BMC Bioinform 9:1–15

    Article  Google Scholar 

  • Schofield R, Taylor AW (1955) The measurement of soil pH. Soil Sci Soc America J 19:164–167

    Article  CAS  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genom Biol 12:1–18

    Article  Google Scholar 

  • Shea MM, Kuppermann J, Rogers MP, Smith DS, Edwards P, Boehm AB (2023) Systematic review of marine environmental DNA metabarcoding studies: toward best practices for data usability and accessibility. PeerJ 11:e14993

    Article  PubMed  PubMed Central  Google Scholar 

  • Shiau Y-J, Chiu C-Y (2020) Biogeochemical processes of C and N in the soil of mangrove forest ecosystems. Forests 11:492

    Article  Google Scholar 

  • Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161. https://doi.org/10.1128/AEM.02345-10

    Article  CAS  PubMed  Google Scholar 

  • Smith MW, Zeigler Allen L, Allen AE, Herfort L, Simon HM (2013) Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Front Microbiol 4:120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992–1000

    Article  CAS  PubMed  Google Scholar 

  • Steele HL, Streit WR (2005) Metagenomics: advances in ecology and biotechnology. FEMS Microbiol Lett 247:105–111. https://doi.org/10.1016/j.femsle.2005.05.011

    Article  CAS  PubMed  Google Scholar 

  • Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160. https://doi.org/10.1128/JB.00345-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suwa R, Deshar R, Hagihara A (2009) Forest structure of a subtropical mangrove along a river inferred from potential tree height and biomass. Aquat Bot 91:99–104

    Article  Google Scholar 

  • Thompson CE, Beys-da-Silva WO, Santi L, Berger M, Vainstein MH, Guima Raes JA, Vasconcelos AT (2013) A potential source for cellulolytic enzyme discovery and environmental aspects revealed through metagenomics of Brazilian mangroves. AMB Express 3:65. https://doi.org/10.1186/2191-0855-3-65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari N, Bansal M, Sharma JG (2021) Metagenomics: a powerful lens viewing the microbial world. In Wastewater Treatment Reactors. Elsevier, pp 309–339

    Chapter  Google Scholar 

  • Vazquez P, Holguin G, Puente M, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    Article  CAS  Google Scholar 

  • Vieira RP, Gonzalez AM, Cardoso AM, Oliveira DN, Albano RM, Clementino MM, Martins OB, Paranhos R (2008) Relationships between bacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environ Microbiol 10:189–199

    Article  CAS  PubMed  Google Scholar 

  • Wakley A, Black C (1934) Determination of organic matter in the soil by chromic acid digesion. Soil Sci 63:251–264

    Google Scholar 

  • Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils—effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264

    Article  CAS  Google Scholar 

  • Wang S, Hou W, Dong H, Jiang H, Huang L, Wu G, Zhang C, Song Z, Zhang Y, Ren H, Zhang J, Zhang L (2013) Control of temperature on microbial community structure in hot springs of the Tibetan Plateau. PLoS ONE 8:e62901. https://doi.org/10.1371/journal.pone.0062901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wee AKS, Mori GM, Lira CF, Núñez-Farfán J, Takayama K, Faulks L, Shi S, Tsuda Y, Suyama Y, Yamamoto T, Iwasaki T, Nagano Y, Wang Z, Watanabe S, Kajita T (2019) The integration and application of genomic information in mangrove conservation. Conserv Biol 33:206–209. https://doi.org/10.1111/cobi.13140

    Article  PubMed  Google Scholar 

  • Wu P, Xiong X, Xu Z, Lu C, Cheng H, Lyu X, Zhang J, He W, Deng W, Lyu Y, Lou Q, Hong Y, Fang H (2016) Bacterial communities in the rhizospheres of three mangrove tree species from Beilun Estuary, China. PLoS ONE 11:e0164082. https://doi.org/10.1371/journal.pone.0164082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan B, Hong K, Yu ZN (2006) Archaeal communities in mangrove soil characterized by 16S rRNA gene clones. J Microbiol 44:566–571

    CAS  PubMed  Google Scholar 

  • Yang J, Gao J, Cheung A, Liu B, Schwendenmann L, Costello MJ (2013) Vegetation and sediment characteristics in an expanding mangrove forest in New Zealand. Estuar Coast Shelf Sci 134:11–18. https://doi.org/10.1016/j.ecss.2013.09.017

    Article  CAS  Google Scholar 

  • Yeo SK, Huggett MJ, Eiler A, Rappé MS (2013) Coastal bacterioplankton community dynamics in response to a natural disturbance. PLoS ONE 8:e56207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan SY, Chang BV (2007) Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. J Environ Sci Health B 42:63–69

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163. https://doi.org/10.1099/ijs.0.02520-0

    Article  CAS  PubMed  Google Scholar 

  • Zulfa A, Norizah K, Hamdan O, Faridah-Hanum I, Rhyma P, Fitrianto A (2021) Spectral signature analysis to determine mangrove species delineation structured by anthropogenic effects. Ecol Indic 130:108148

    Article  Google Scholar 

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Funding

The work is supported in part under Xinjiang Uygur Autonomous Region, regional coordinated Innovation Project and Shanghai Cooperation Organization Science and Technology Partnership Program China (No. 2021E01018) and Innovation Group Project of Southern Marine Science andEngineering Guangdong Laboratory (Zhuhai) (Nos. 311021004, 311021006). The research was also supported by the Chinese Academy of Sciences President’s International Fellowship Initiative (Grant No.2020VBA0020). WJL was also supported by the Introduction project of high-level talents in Xinjiang Uygur Autonomous Region.

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RB, IA, and BU contributed to conception and design of the study. RB collected samples. ME performed physicochemical analysis of soil samples. RB, AAl, SL, ZL, and JL performed the experiments. RB, SL, JL, and IA organized the database. RB, AAl, SL, ZL, JL, and AAm contributed to the statistical data analysis and finalizing the figures. RB, AAl, AAm, and IA wrote the first draft of the manuscript. AAm, AAl, JL, and YHL wrote sections of the manuscript. IA and WJL managed funds for research and supervised the experiments. All the authors contributed to manuscript revision, read, and approved the submitted version.

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Correspondence to Iftikhar Ahmed or Wen‑Jun Li.

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Bushra, R., Ahmed, I., Li, JL. et al. Untapped rich microbiota of mangroves of Pakistan: diversity and community compositions. Folia Microbiol (2023). https://doi.org/10.1007/s12223-023-01095-3

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