Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition.
Dredged sediments
Lagoon contamination
Manila clam
Microbiota
Molecular changes
Venice lagoon
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
25 10 2023
25 10 2023
Historique:
received:
01
09
2023
accepted:
17
10
2023
medline:
27
10
2023
pubmed:
26
10
2023
entrez:
25
10
2023
Statut:
epublish
Résumé
The reuse of dredged sediments in ports and lagoons is a big issue as it should not affect the quality and the equilibrium of ecosystems. In the lagoon of Venice, sediment management is of crucial importance as sediments are often utilized to built-up structures necessary to limit erosion. However, the impact of sediment reuse on organisms inhabiting this delicate area is poorly known. The Manila clam is a filter-feeding species of high economic and ecological value for the Venice lagoon experiencing a drastic decline in the last decades. In order to define the molecular mechanisms behind sediment toxicity, we exposed clams to sediments sampled from different sites within one of the Venice lagoon navigable canals close to the industrial area. Moreover, we investigated the impacts of dredged sediments on clam's microbial communities. Concentrations of the trace elements and organic chemicals showed increasing concentrations from the city of Venice to sites close to the industrial area of Porto Marghera, where PCDD/Fs and PCBs concentrations were up to 120 times higher than the southern lagoon. While bioaccumulation of organic contaminants of industrial origin reflected sediments' chemical concentrations, metal bioaccumulation was not consistent with metal concentrations measured in sediments probably due to the activation of ABC transporters. At the transcriptional level, we found a persistent activation of the mTORC1 signalling pathway, which is central in the coordination of cellular responses to chemical stress. Microbiota characterization showed the over-representation of potential opportunistic pathogens following exposure to the most contaminated sediments, leading to host immune response activation. Despite the limited acquisition of new microbial species from sediments, the latter play an important role in shaping Manila clam microbial communities. Sediment management in the Venice lagoon will increase in the next years to maintain and create new canals as well as to allow the operation of the new mobile gates at the three Venice lagoon inlets. Our data reveal important transcriptional and microbial changes of Manila clams after exposure to sediments, therefore reuse of dredged sediments represents a potential risk for the conservation of this species and possibly for other organisms inhabiting the Venice lagoon.
Sections du résumé
BACKGROUND
The reuse of dredged sediments in ports and lagoons is a big issue as it should not affect the quality and the equilibrium of ecosystems. In the lagoon of Venice, sediment management is of crucial importance as sediments are often utilized to built-up structures necessary to limit erosion. However, the impact of sediment reuse on organisms inhabiting this delicate area is poorly known. The Manila clam is a filter-feeding species of high economic and ecological value for the Venice lagoon experiencing a drastic decline in the last decades. In order to define the molecular mechanisms behind sediment toxicity, we exposed clams to sediments sampled from different sites within one of the Venice lagoon navigable canals close to the industrial area. Moreover, we investigated the impacts of dredged sediments on clam's microbial communities.
RESULTS
Concentrations of the trace elements and organic chemicals showed increasing concentrations from the city of Venice to sites close to the industrial area of Porto Marghera, where PCDD/Fs and PCBs concentrations were up to 120 times higher than the southern lagoon. While bioaccumulation of organic contaminants of industrial origin reflected sediments' chemical concentrations, metal bioaccumulation was not consistent with metal concentrations measured in sediments probably due to the activation of ABC transporters. At the transcriptional level, we found a persistent activation of the mTORC1 signalling pathway, which is central in the coordination of cellular responses to chemical stress. Microbiota characterization showed the over-representation of potential opportunistic pathogens following exposure to the most contaminated sediments, leading to host immune response activation. Despite the limited acquisition of new microbial species from sediments, the latter play an important role in shaping Manila clam microbial communities.
CONCLUSIONS
Sediment management in the Venice lagoon will increase in the next years to maintain and create new canals as well as to allow the operation of the new mobile gates at the three Venice lagoon inlets. Our data reveal important transcriptional and microbial changes of Manila clams after exposure to sediments, therefore reuse of dredged sediments represents a potential risk for the conservation of this species and possibly for other organisms inhabiting the Venice lagoon.
Identifiants
pubmed: 37880625
doi: 10.1186/s12915-023-01741-9
pii: 10.1186/s12915-023-01741-9
pmc: PMC10601118
doi:
Substances chimiques
Dibenzofurans
0
Water Pollutants, Chemical
0
Polychlorinated Dibenzodioxins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
234Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Mol Cell Biol. 2004 Jan;24(1):200-16
pubmed: 14673156
Environ Toxicol Chem. 2021 Jun;40(6):1586-1595
pubmed: 33523501
Arch Biochem Biophys. 2001 Jun 15;390(2):149-57
pubmed: 11396917
Environ Sci Pollut Res Int. 2016 Jun;23(11):10556-10565
pubmed: 26780047
Essays Biochem. 2017 Dec 12;61(6):565-584
pubmed: 29233869
Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15552-7
pubmed: 17028174
PLoS One. 2016 Mar 03;11(3):e0150184
pubmed: 26938082
Int J Mol Cell Med. 2015 Winter;4(1):1-8
pubmed: 25815277
Front Cell Dev Biol. 2022 Aug 19;10:920683
pubmed: 36060812
Genomics. 2021 Jan;113(1 Pt 2):944-956
pubmed: 33127583
Aquat Toxicol. 2018 Jan;194:195-207
pubmed: 29202271
J Biol Chem. 2007 Aug 10;282(32):23679-86
pubmed: 17553806
Nat Rev Mol Cell Biol. 2004 Sep;5(9):687-98
pubmed: 15340377
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Aquat Toxicol. 2017 Feb;183:94-103
pubmed: 28040644
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Curr Opin Cell Biol. 2009 Dec;21(6):825-36
pubmed: 19767189
PLoS One. 2013 Apr 22;8(4):e61217
pubmed: 23630581
Methods Mol Biol. 2014;1170:113-44
pubmed: 24906312
Environ Microbiol Rep. 2010 Feb;2(1):34-43
pubmed: 23765996
Nat Cell Biol. 2011 Feb;13(2):132-41
pubmed: 21258367
Chem Biol Interact. 2012 Jun 25;198(1-3):9-17
pubmed: 22580103
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Mol Cell. 2016 Feb 18;61(4):625-639
pubmed: 26876939
Eur J Med Chem. 2020 Dec 15;208:112820
pubmed: 32966896
J Fish Dis. 2018 Feb;41(2):215-221
pubmed: 28836671
Dis Aquat Organ. 2006 Aug 30;71(3):255-66
pubmed: 17058606
Toxicol Sci. 2004 Dec;82(2):436-42
pubmed: 15375296
Arch Pharm Res. 2009 Jun;32(6):883-91
pubmed: 19557366
Aquat Toxicol. 2018 Feb;195:114-128
pubmed: 29306034
Mar Pollut Bull. 2007;55(10-12):529-42
pubmed: 17963790
Nature. 1997 May 22;387(6631):422-6
pubmed: 9163430
Bull Environ Contam Toxicol. 2013 Mar;90(3):387-90
pubmed: 23275976
Aquat Toxicol. 2015 Feb;159:156-66
pubmed: 25546006
Environ Pollut. 2022 Aug 15;307:119502
pubmed: 35605833
Hepatology. 2017 Jul;66(1):167-181
pubmed: 28370287
Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):11988-93
pubmed: 23803853
Mar Pollut Bull. 2017 Nov 15;124(1):121-129
pubmed: 28712769
Sci Rep. 2020 Nov 11;10(1):19531
pubmed: 33177569
ISME J. 2015 Mar;9(3):670-82
pubmed: 25180968
J Physiol. 2002 Jul 1;542(Pt 1):3-16
pubmed: 12096044
J Comp Physiol B. 2008 Nov;178(8):935-55
pubmed: 18594835
Genes Dev. 1998 Aug 1;12(15):2245-62
pubmed: 9694791
Am J Physiol Renal Physiol. 2015 Feb 1;308(3):F267-74
pubmed: 25428129
BMC Genomics. 2016 Oct 25;17(Suppl 8):727
pubmed: 27801296
Sci Total Environ. 2002 Aug 5;295(1-3):35-49
pubmed: 12186291
Cell. 2017 Mar 9;168(6):960-976
pubmed: 28283069
Cell. 2000 Oct 13;103(2):253-62
pubmed: 11057898
Environ Res. 2020 Mar;182:108984
pubmed: 31830695
Environ Microbiol. 2010 Jul;12(7):2007-19
pubmed: 20370818
Int Microbiol. 2009 Jun;12(2):107-14
pubmed: 19784930
Environ Int. 2021 Jul;152:106484
pubmed: 33740673
Oncogene. 2008 Jul 10;27(30):4172-9
pubmed: 18345030
Aquat Toxicol. 2016 May;174:123-33
pubmed: 26945539
Cell Syst. 2015 Dec 23;1(6):417-425
pubmed: 26771021
Nature. 2000 Nov 23;408(6811):433-9
pubmed: 11100718
PeerJ. 2017 Nov 29;5:e4106
pubmed: 29201571
Sci Rep. 2019 Apr 29;9(1):6615
pubmed: 31036875
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Mar Pollut Bull. 2006 Dec;52(12):1553-72
pubmed: 17078974
Oncogene. 2018 Sep;37(38):5205-5220
pubmed: 29849119
Microbiol Mol Biol Rev. 2002 Dec;66(4):579-91, table of contents
pubmed: 12456783
Environ Pollut. 2012 Dec;171:52-60
pubmed: 22871644
Cell Rep. 2015 Nov 3;13(5):944-56
pubmed: 26565908
Comp Biochem Physiol B Biochem Mol Biol. 2015 Dec;190:8-15
pubmed: 26310361
Bioessays. 2017 May;39(5):
pubmed: 28295473
Cell Logist. 2017 Sep 29;7(4):e1378794
pubmed: 29296509
Environ Sci Technol. 2005 Apr 1;39(7):1921-31
pubmed: 15871220
Sci Total Environ. 2022 Apr 20;818:151712
pubmed: 34800444
Evol Appl. 2021 Nov 27;14(12):2864-2880
pubmed: 34950234
ISME J. 2013 May;7(5):991-1002
pubmed: 23283017
Annu Rev Genet. 2006;40:209-35
pubmed: 16805667
FEMS Microbiol Ecol. 2014 Jan;87(1):268-79
pubmed: 24112035
Aquat Toxicol. 2015 Sep;166:10-20
pubmed: 26186662
Biometals. 2010 Oct;23(5):857-75
pubmed: 20204475
Toxicol Appl Pharmacol. 2008 May 15;229(1):10-9
pubmed: 18295293
Front Microbiol. 2015 Sep 16;6:989
pubmed: 26441918
J Cell Biol. 2000 Dec 11;151(6):1207-20
pubmed: 11121436
Appl Environ Microbiol. 2021 Feb 12;87(5):e0258120
pubmed: 33310713
Arch Environ Contam Toxicol. 2012 Jan;62(1):56-67
pubmed: 21526414
Mol Ecol. 2013 Apr;22(8):2157-72
pubmed: 23480613
Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):15790-7
pubmed: 26669439
J Cell Biol. 1996 Nov;135(4):913-24
pubmed: 8922376
J Enzyme Inhib Med Chem. 2013 Feb;28(1):195-204
pubmed: 22299581
Nat Protoc. 2013 Aug;8(8):1494-512
pubmed: 23845962
Arch Toxicol. 2010 Jan;84(1):3-16
pubmed: 20020104
J Cell Biol. 2019 Sep 2;218(9):3019-3038
pubmed: 31431476
Mol Cell. 2001 Jul;8(1):105-13
pubmed: 11511364
J Exp Biol. 2009 Aug;212(Pt 16):2627-34
pubmed: 19648408
Trends Cell Biol. 2014 Jul;24(7):400-6
pubmed: 24698685
Nat Commun. 2022 Aug 10;13(1):4685
pubmed: 35948564
Integr Environ Assess Manag. 2007 Jul;3(3):393-414
pubmed: 17695112
Sci Total Environ. 2016 Oct 1;566-567:1362-1367
pubmed: 27267717
Environ Pollut. 2015 Feb;197:90-98
pubmed: 25514060
Genes Dev. 2003 May 1;17(9):1115-29
pubmed: 12695333
Nat Biotechnol. 2019 Aug;37(8):852-857
pubmed: 31341288
Dev Comp Immunol. 2020 Mar;104:103564
pubmed: 31816330