Large-scale differences in diversity and functional adaptations of prokaryotic communities from conserved and anthropogenically impacted mangrove sediments in a tropical estuary

Carolina O. De Santana; Pieter Spealman; Vania Melo; David Gresham; Taise de Jesus; Eddy Oliveira; Fabio Alexandre Chinalia

doi:10.7717/peerj.12229

journal article Open Access Sep 23, 2021

Large-scale differences in diversity and functional adaptations of prokaryotic communities from conserved and anthropogenically impacted mangrove sediments in a tropical estuary

Carolina O. De Santana Pieter Spealman Vania Melo David Gresham Taise de Jesus Eddy Oliveira Fabio Alexandre Chinalia

PeerJ Vol. 9 pp. e12229 · PeerJ

View at Publisher Save 10.7717/peerj.12229

Abstract

Mangroves are tropical ecosystems with strategic importance for climate change mitigation on local and global scales. They are also under considerable threat due to fragmentation degradation and urbanization. However, a complete understanding of how anthropogenic actions can affect microbial biodiversity and functional adaptations is still lacking. In this study, we carried out 16S rRNA gene sequencing analysis using sediment samples from two distinct mangrove areas located within the Serinhaém Estuary, Brazil. The first sampling area was located around the urban area of Ituberá, impacted by domestic sewage and urban runoff, while the second was an environmentally conserved site. Our results show significant changes in the structure of the communities between impacted and conserved sites. Biodiversity, along with functional potentials for the cycling of carbon, nitrogen, phosphorus and sulfur, were significantly increased in the urban area. We found that the environmental factors of organic matter, temperature and copper were significantly correlated with the observed shifts in the communities. Contributions of specific taxa to the functional potentials were negatively correlated with biodiversity, such that fewer numbers of taxa in the conserved area contributed to the majority of the metabolic potential. The results suggest that the contamination by urban runoff may have generated a different environment that led to the extinction of some taxa observed at the conserved site. In their place we found that the impacted site is enriched in prokaryotic families that are known human and animal pathogens, a clear negative effect of the urbanization process.

Topics

No keywords indexed for this article. Browse by subject →

References

87

[1]

Affe "Metagenomic analysis of cyanobacteria in an oligotrophic tropical estuary, South Atlantic" Frontiers in Microbiology (2018) 10.3389/fmicb.2018.01393

[2]

Allard "Introducing the mangrove microbiome initiative: identifying microbial research priorities and approaches to better understand, protect, and rehabilitate mangrove ecosystems" MSystems (2020) 10.1128/msystems.00658-20

[3]

Andrei "Niche-directed evolution modulates genome architecture in freshwater Planctomycetes" The ISME Journal (2019) 10.1038/s41396-018-0332-5

[4]

Distance‐Based Tests for Homogeneity of Multivariate Dispersions

Marti J. Anderson

Biometrics 2006 10.1111/j.1541-0420.2005.00440.x

[5]

Andreote "The microbiome of Brazilian mangrove sediments as revealed by metagenomics" PLOS ONE (2012) 10.1371/journal.pone.0038600

[6]

Aoyagi "Dynamic transition of chemolithotrophic sulfur-oxidizing bacteria in response to amendment with nitrate in deposited marine sediments" Frontiers in Microbiology (2015) 10.3389/fmicb.2015.00426

[7]

Barbera "EPA-ng: massively parallel evolutionary placement of genetic sequences" Systematic Biology (2019) 10.1093/sysbio/syy054

[8]

Barnes "Predicting microbiome function across space is confounded by strain-level differences and functional redundancy across taxa" Frontiers in Microbiology (2020) 10.3389/fmicb.2020.00101

[9]

Biddle "Untangling the genetic basis of fibrolytic specialization by lachnospiraceae and ruminococcaceae in diverse gut communities" Diversity (2013) 10.3390/d5030627

[10]

Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin

Nicholas A. Bokulich, Benjamin D. Kaehler, Jai Ram Rideout et al.

Microbiome 2018 10.1186/s40168-018-0470-z

[11]

Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel

Bioinformatics 2014 10.1093/bioinformatics/btu170

[12]

Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2

Evan Bolyen, Jai Ram Rideout, Matthew R. Dillon et al.

Nature Biotechnology 2019 10.1038/s41587-019-0209-9

[13]

Bulseco "Nitrate addition stimulates microbial decomposition of organic matter in salt marsh sediments" Global Change Biology (2019) 10.1111/gcb.14726

[14]

Cabral "Anthropogenic impact on mangrove sediments triggers differential responses in the heavy metals and antibiotic resistomes of microbial communities" Environmental Pollution (2016) 10.1016/j.envpol.2016.05.078

[15]

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms

J Gregory Caporaso, Christian L Lauber, William A Walters et al.

The ISME Journal 2012 10.1038/ismej.2012.8

[16]

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample

J. Gregory Caporaso, Christian L. Lauber, William A. Walters et al.

Proceedings of the National Academy of Sciences 2011 10.1073/pnas.1000080107

[17]

Carneiro "Evaluation of the concentrations of elements at trace level in the Serinhaem River estuary, Bahia, Brazil, using chemometric tools" Marine Pollution Bulletin (2021) 10.1016/j.marpolbul.2020.111953

[18]

Christensen "The family Pasteurellaceae" The Prokaryotes (2014) 10.1007/978-3-642-38922-1_224

[19]

Coenye "The family Burkholderiaceae" (2014) 10.1007/978-3-642-30197-1_239

[20]

CONAMA "Conselho Nacional De Meio Ambiente. 2002. Resolução CONAMA no. 303, de 20 de março de 2002" (2002)

[21]

Craig "Nitrogen addition alters composition, diversity, and functioning of microbial communities in mangrove soils: an incubation experiment" Soil Biology & Biochemistry (2021) 10.1016/j.soilbio.2020.108076

[22]

Czech "Genesis and Gappa: processing, analyzing and visualizing phylogenetic (placement) data" Bioinformatics (2020) 10.1093/bioinformatics/btaa070

[23]

Ditt "Conservação da biodiversidade por meio da atividade extrativista em comunidades quilombolas" Revista Brasileira de Ciências Ambientais (2013)

[24]

Dixon "VEGAN, a package of R functions for community ecology" Journal of Vegetation Science (2003) 10.1658/1100-9233(2003)014[0927:vaporf]2.0.co;2

[25]

Dong "Source, structural characteristics and ecological indication of dissolved organic matter extracted from sediments in the primary tributaries of the Dagu River" Ecological Indicators (2020) 10.1016/j.ecolind.2019.105776

[26]

Douglas "PICRUSt2: an improved and extensible approach for metagenome inference" BioRxiv (2019) 10.1101/672295

[27]

Eberhard "Oxidation of polymetal sulfides by chemolithoautotrophic bacteria from deep-sea hydrothermal vents" Geomicrobiology Journal (1995) 10.1080/01490459509378014

[28]

Farmer "The family Vibrionaceae" (2006) 10.1007/0-387-30746-x_17

[29]

Fernandes "Bacterial diversity in relatively pristine and anthropogenically-influenced mangrove ecosystems (Goa, India)" Brazilian Journal of Microbiology (2014) 10.1590/s1517-83822014000400006

[30]

Filippino "The bioavailability of effluent-derived organic nitrogen along an estuarine salinity gradient" Estuaries and Coasts: Journal of the Estuarine Research Federation (2011) 10.1007/s12237-010-9314-1

[31]

Status and distribution of mangrove forests of the world using earth observation satellite data

C. Giri, E. Ochieng, L. L. Tieszen et al.

Global Ecology and Biogeography 2011 10.1111/j.1466-8238.2010.00584.x

[32]

Glibert "Eutrophication, harmful algae and biodiversity - Challenging paradigms in a world of complex nutrient changes" Marine Pollution Bulletin (2017) 10.1016/j.marpolbul.2017.04.027

[33]

Gong "High-throughput sequencing and analysis of microbial communities in the mangrove swamps along the coast of Beibu Gulf in Guangxi, China" Scientific Reports (2019) 10.1038/s41598-019-45804-w

[34]

Houser "Nitrogen and phosphorus in the upper Mississippi river: transport, processing, and effects on the river ecosystem" Hydrobiologia (2010) 10.1007/s10750-009-0067-4

[35]

Howard "Clarifying the role of coastal and marine systems in climate mitigation" Frontiers in Ecology and the Environment (2017) 10.1002/fee.1451

[36]

IBGE – INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA (2020)

[37]

Imchen "Metagenomic insights into the antibiotic resistome of mangrove sediments and their association to socioeconomic status" Environmental Pollution (2021) 10.1016/j.envpol.2020.115795

[38]

Imchen "Searching for signatures across microbial communities: Metagenomic analysis of soil samples from mangrove and other ecosystems" Scientific Reports (2017) 10.1038/s41598-017-09254-6

[39]

Imchen "Comparative mangrove metagenome reveals global prevalence of heavy metals and antibiotic resistome across different ecosystems" Scientific Reports (2018) 10.1038/s41598-018-29521-4

[40]

Jovel "Characterization of the Gut Microbiome Using 16S or Shotgun Metagenomics" Frontiers in Microbiology (2016) 10.3389/fmicb.2016.00459

[41]

Kanehisa "KEGG Mapper for inferring cellular functions from protein sequences" Protein Science (2020) 10.1002/pro.3711

[42]

Karami "The phylum Spirochaetaceae" (2014) 10.1007/978-3-642-38954-2_156

[43]

The Ecology of Acidobacteria: Moving beyond Genes and Genomes

Anna M. Kielak, Cristine C. Barreto, George A. Kowalchuk et al.

Frontiers in Microbiology 2016 10.3389/fmicb.2016.00744

[44]

Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform

James J. Kozich, Sarah L. Westcott, Nielson T. Baxter et al.

Applied and Environmental Microbiology 2013 10.1128/aem.01043-13

[45]

Krauss "Environmental Drivers in Mangrove Establishment and Early Development: A Review" Aquatic Botany (2008) 10.1016/j.aquabot.2007.12.014

[46]

Kristensen "High diversity and functional potential of undescribed “Acidobacteriota” in danish wastewater treatment plants" Frontiers in Microbiology (2021) 10.3389/fmicb.2021.643950

[47]

Lin "Mangrove sediment microbiome: adaptive microbial assemblages and their routed biogeochemical processes in yunxiao mangrove national nature reserve, China" Microbial Ecology (2019) 10.1007/s00248-018-1261-6

[48]

Liu "Syntrophobacteraceae-affiliated species are major propionate-degrading sulfate reducers in paddy soil" Environmental Microbiology (2017) 10.1111/1462-2920.13698

[49]

Lopes "Análise da paisagem com base na fragmentação - caso APA do Pratigi, baixo sul da Bahia, Brasil" Revista Eletrônica do Prodema (2011)

[50]

Louca "Efficient comparative phylogenetics on large trees" Bioinformatics (2018) 10.1093/bioinformatics/btx701

Showing 50 of 87 references

Metrics

16

Citations

87

References

Details

Published: Sep 23, 2021
Vol/Issue: 9
Pages: e12229
License: View

Authors

C

Carolina O. De Santana

Geosciences Institute, Federal University of Bahia, Salvador, Bahia, Brazil

P

Pieter Spealman

Department of Biology, New York University, New York City, NY, United States of America

V

Vania Melo

Department of Biology, Federal University of Ceará, Fortaleza, Ceará, Brazil

D

David Gresham

Department of Biology, New York University, New York City, NY, United States of America

T

Taise de Jesus

Department of Biology, State University of Feira de Santana, Feira de Santana, Bahia, Brazil

E

Eddy Oliveira

Department of Biology, State University of Feira de Santana, Feira de Santana, Bahia, Brazil

F

Fabio Alexandre Chinalia

Geosciences Institute, Federal University of Bahia, Salvador, Bahia, Brazil

Funding

Fundação de Amparo à Pesquisa do Estado da Bahia – Fapesb Award: 19.571.128.2566

Cite This Article

Carolina O. De Santana, Pieter Spealman, Vania Melo, et al. (2021). Large-scale differences in diversity and functional adaptations of prokaryotic communities from conserved and anthropogenically impacted mangrove sediments in a tropical estuary. PeerJ, 9, e12229. https://doi.org/10.7717/peerj.12229

Large-scale differences in diversity and functional adaptations of prokaryotic communities from conserved and anthropogenically impacted mangrove sediments in a tropical estuary

You May Also Like