DOI: https://doi.org/10.3354/meps14866
copiedMicrobial structural shifts and enhanced carbon metabolism following coral restoration on Wuzhizhou Island, China
ABSTRACT:
Global climate change and human activities are accelerating coral reef degradation, prompting extensive coral restoration efforts. However, how coral restoration influences microbial community structure and function remains unclear. We examined the ecological impacts of coral restoration on Wuzhizhou Island, Hainan, China, by comparing the microbial community structures and metabolic functions in seawater and sediment from natural, degraded, and restored sites. Results showed that microbial communities in both seawater and sediment were dominated by specific bacterial groups. Fluviicola was abundant in natural seawater, while Owenweeksia and Desulfosarcina were prevalent in fragmented areas. Candidatus Pelagibacter and Hyphomonas were abundant in restored areas. Bacterial richness, diversity, and interrelationships varied significantly across these environments. Restoration efforts markedly enhanced microbial carbon metabolism in seawater and sediment, with clear recovery in the citric acid cycle and pentose phosphate pathways. However, linear discriminant analysis effect size suggested an enrichment of pathogen-associated pathways in restored sediment, indicating that human-induced ecological disturbances could affect microbial metabolic functions in sediment. While coral restoration notably enhanced microbial community structure and carbon metabolism in seawater, sediment functional recovery was slower, highlighting the environmental complexities and challenges of restoring microbial functions in both environments and provided key insights for improving coral restoration strategies.
KEYWORDS
Aliashkevich A, Guest T, Alvarez L, Gilmore MC and others (2024) LD-transpeptidation is crucial for fitness and polar growth in Agrobacterium tumefaciens. PLOS Genet 20:e1011449 PubMed Crossref
Becker DM, Silbiger NJ (2020) Nutrient and sediment loading affect multiple facets of functionality in a tropical branching coral. J Exp Biol 223:jeb225045 PubMed Crossref
Beese CM, Mumby PJ, Rogers A (2023) Small-scale habitat complexity preserves ecosystem services on coral reefs. J Appl Ecol 60:1854-1867 Crossref
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59-60 PubMed Crossref
Che S, Huang M, Ma H, Wan Z, Feng J, Ding S, Li X (2024) Toxic effects of nanopolystyrene and cadmium on the intestinal tract of the Chinese mitten crab (Eriocheir sinensis). Ecotoxicol Environ Saf 270:115936 PubMed Crossref
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884-i890 PubMed Crossref
Chen SC, Ji J, Popp D, Jaekel U, Richnow HH, Sievert SM, Musat F (2022) Genome and proteome analyses show the gaseous alkane degrader Desulfosarcina sp. strain BuS5 as an extreme metabolic specialist. Environ Microbiol 24:1964-1976 PubMed Crossref
Chiarello M, Auguet JC, Graham NAJ, Claverie T and others (2020) Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes. Proc R Soc B 287:20200642 Crossref PubMed
Conover AE, Morando M, Zhao Y, Semones J, Hutchins DA, Webb EA (2021) Alphaproteobacteria facilitate Trichodesmium community trimethylamine utilization. Environ Microbiol 23:6798-6810 PubMed Crossref
Cook KM, Yamagiwa H, Beger M, Masucci GD and others (2022) A community and functional comparison of coral and reef fish assemblages between four decades of coastal urbanisation and thermal stress. Ecol Evol 12:e8736 PubMed Crossref
Cornwall CE, Comeau S, DeCarlo TM, Larcombe E and others (2020) A coralline alga gains tolerance to ocean acidification over multiple generations of exposure. Nat Clim Change 10:143-146 Crossref
da Cunha ICM, da Silva AVR, Boleta EHM, Pellegrinetti TA and others (2024) The interplay between the inoculation of plant growth-promoting rhizobacteria and the rhizosphere microbiome and their impact on plant phenotype. Microbiol Res 283:127706 PubMed Crossref
Doering T, Tandon K, Topa SH, Pidot SJ, Blackall LL, van Oppen MJH (2023) Genomic exploration of coral-associated bacteria: identifying probiotic candidates to increase coral bleaching resilience in Galaxea fascicularis. Microbiome 11:185 PubMed Crossref
Edmunds PJ, Aronson RB, Swanson DW, Levitan DR, Precht WF (1998) Photographic versus visual census techniques for the quantification of juvenile corals. Bull Mar Sci 62:937-946
França FM, Benkwitt CE, Peralta G, Robinson JPW and others (2020) Climatic and local stressor interactions threaten tropical forests and coral reefs. Philos Trans R Soc B 375:20190116 PubMed Crossref
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150-3152 PubMed Crossref
Glasl B, Bourne DG, Frade PR, Thomas T, Schaffelke B, Webster NS (2019) Microbial indicators of environmental perturbations in coral reef ecosystems. Microbiome 7:94 PubMed Crossref
Haas AF, Fairoz MFM, Kelly LW, Nelson CE and others (2016) Global microbialization of coral reefs. Nat Microbiol 1:16042 PubMed Crossref
Howard RD, Schul MD, Rodriguez Bravo LM, Altieri AH, Meyer JL (2023) Shifts in the coral microbiome in response to in situ experimental deoxygenation. Appl Environ Microbiol 89:e00577-23 PubMed Crossref
Hurst NR, Locher B, Steinmuller HE, Walters LJ, Chambers LG (2022) Organic carbon dynamics and microbial community response to oyster reef restoration. Limnol Oceanogr 67:1157-1168 Crossref
Iacarella JC, Adamczyk E, Bowen D, Chalifour L and others (2018) Anthropogenic disturbance homogenizes seagrass fish communities. Glob Change Biol 24:1904-1918 PubMed Crossref
Kanekar PP, Kulkarni SO, Kanekar SP, Shouche Y, Jani K, Sharma A (2015) Exploration of a haloarchaeon, Halostagnicola larsenii, isolated from rock pit sea water, west coast of Maharashtra, India, for the production of bacteriorhodopsin. J Appl Microbiol 118:1345-1356 PubMed Crossref
Klingner A, Bartsch A, Dogs M, Wagner-Döbler I and others (2015) Large-scale 13C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81:2408-2422 PubMed Crossref
Lamont TAC, Williams B, Chapuis L, Prasetya ME and others (2022) The sound of recovery: Coral reef restoration success is detectable in the soundscape. J Appl Ecol 59:742-756 Crossref
Lee J, Yang JH, Weber APM, Bhattacharya D, Kim WY, Yoon HS (2024) Diurnal rhythms in the red seaweed Gracilariopsis chorda are characterized by unique regulatory networks of carbon metabolism. Mol Biol Evol 41:msae012 PubMed Crossref
Levy N, Marques JA, Simon-Blecher N, Bourne DG and others (2024) Ecosystem transplant from a healthy reef boosts coral health at a degraded reef. Nat Commun 15:10033 PubMed Crossref
Li D, Liu C, Luo R, Sadakane K, Lam TW (2015) MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674-1676 PubMed Crossref
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713-714 PubMed Crossref
Li ZR, Zhang XN, Wang HC, Cheng HY and others (2023) Effects of salinity on sulfur-dominated autotrophic denitrification microorganisms: microbial community succession, key microorganisms and response mechanisms. Chem Eng J 478:147308 Crossref
Liu X, Zhu W, Chen R, Rinkevich B and others (2024) Framed reef modules: a new and cost-effective tool for coral restoration. Restor Ecol 32:e13997 Crossref
Marangon E, Laffy PW, Bourne DG, Webster NS (2021) Microbiome-mediated mechanisms contributing to the environmental tolerance of reef invertebrate species. Mar Biol 168:89 Crossref
Matthews JL, Raina JB, Kahlke T, Seymour JR, van Oppen MJH, Suggett DJ (2020) Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks. Environ Microbiol 22:1675-1687 PubMed Crossref
Mera H, Bourne DG (2018) Disentangling causation: complex roles of coral-associated microorganisms in disease. Environ Microbiol 20:431-449 PubMed Crossref
Moreno-Ulloa A, Sicairos Diaz V, Tejeda-Mora JA, Macias Contreras MI and others (2020) Chemical profiling provides insights into the metabolic machinery of hydrocarbon-degrading deep-sea microbes. mSystems 5:e00824-20 PubMed Crossref
Mueller B, Brocke HJ, Rohwer FL, Dittmar T, Huisman J, Vermeij MJA, de Goeij JM (2022) Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs. Funct Ecol 36:2104-2118 PubMed Crossref
Nelson CE, Wegley Kelly L, Haas AF (2023) Microbial interactions with dissolved organic matter are central to coral reef ecosystem function and resilience. Annu Rev Mar Sci 15:431-460 PubMed Crossref
Niu L, Guo Y, Li Y, Wang C and others (2021) Degradation of river ecological quality in Tibet Plateau with overgrazing: a quantitative assessment using biotic integrity index improved by random forest. Ecol Indic 120:106948 Crossref
Nogales B, Lanfranconi MP, Piña-Villalonga JM, Bosch R (2011) Anthropogenic perturbations in marine microbial communities. FEMS Microbiol Rev 35:275-298 PubMed Crossref
Noguchi H, Park J, Takagi T (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34:5623-5630 PubMed Crossref
Opara CB, Kamariah N, Spooren J, Pollmann K, Kutschke S (2023) Interesting halophilic sulphur-oxidising bacteria with bioleaching potential: implications for pollutant mobilization from mine waste. Microorganisms 11:222 PubMed Crossref
Oshiki M, Toyama Y, Suenaga T, Terada A, Kasahara Y, Yamaguchi T, Araki N (2022) N2O reduction by Gemmatimonas aurantiaca and potential involvement of Gemmatimonadetes bacteria in N2O reduction in agricultural soils. Microbes Environ 37:ME21090 Crossref
Perera-Valderrama S, Hernández-Ávila A, Ferro-Azcona H, Cobián-Rojas D and others (2020) Increasing marine ecosystems conservation linking marine protected areas and integrated coastal management in southern Cuba. Ocean Coast Manage 196:105300 Crossref
Pierrot DE, Lewis E, Wallace DWR (2006) MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN
Randall CJ, Negri AP, Quigley KM, Foster T and others (2020) Sexual production of corals for reef restoration in the Anthropocene. Mar Ecol Prog Ser 635:203-232 Crossref
Ricci F, Tandon K, Moßhammer M, Cho EHJ, Blackall LL, Kühl M, Verbruggen H (2023) Fine-scale mapping of physicochemical and microbial landscapes of the coral skeleton. Environ Microbiol 25:1505-1521 PubMed Crossref
Romano S, Schulz-Vogt HN, González MJ, Bondarev V (2015) Phosphate limitation induces drastic physiological changes, virulence-related gene expression, and secondary metabolite production in Pseudovibrio sp. strain FO-BEG1. Appl Environ Microbiol 81:3518-3528 PubMed Crossref
Shah RM, Hillyer KE, Stephenson S, Crosswell J and others (2021) Functional analysis of pristine estuarine marine sediments. Sci Total Environ 781:146526 PubMed Crossref
Shore-Maggio A, Aeby GS, Callahan SM (2018) Influence of salinity and sedimentation on Vibrio infection of the Hawaiian coral Montipora capitata. Dis Aquat Org 128:63-71 PubMed Crossref
Song W, Lu H, Li Q, Wang X, Fu Z, Zhou J (2023) Aerobic degradation of ketoprofen by marine consortia: Fenton-like reaction and degradation pathway. Sci Total Environ 892:164520 PubMed Crossref
Sowell SM, Norbeck AD, Lipton MS, Nicora CD and others (2008) Proteomic analysis of stationary phase in the marine bacterium ‘Candidatus Pelagibacter ubique’. Appl Environ Microbiol 74:4091-4100 PubMed Crossref
Srinivasan R, Kannappan A, Shi C, Lin X (2021) Marine bacterial secondary metabolites: a treasure house for structurally unique and effective antimicrobial compounds. Mar Drugs 19:530 PubMed Crossref
Strazzulli A, Fusco S, Cobucci-Ponzano B, Moracci M, Contursi P (2017) Metagenomics of microbial and viral life in terrestrial geothermal environments. Rev Environ Sci Biotechnol 16:425-454 Crossref
Taenzer L (2024) Dynamics and implications of ROS in marine systems. PhD dissertation, Massachusetts Institute of Technology, Cambridge, MA Link
Van Campenhout J, Vanreusel A, Van Belleghem S, Derycke S (2016) Transcription, signaling receptor activity, oxidative phosphorylation, and fatty acid metabolism mediate the presence of closely related species in distinct intertidal and cold-seep habitats. Genome Biol Evol 8:51-69 PubMed Crossref
Wang L, Liang Z, Chai Z, Cong W and others (2025) Construction and evolution of artificial reef ecosystems: response and regulation of marine microorganisms. Environ Pollut 367:125610 PubMed Crossref
Watanabe M, Higashioka Y, Kojima H, Fukui M (2017) Desulfosarcina widdelii sp. nov. and Desulfosarcina alkanivorans sp. nov., hydrocarbon-degrading sulfate-reducing bacteria isolated from marine sediment and emended description of the genus Desulfosarcina. Int J Syst Evol Microbiol 67:2994-2997 PubMed Crossref
Watanabe T, Kubo K, Kamei Y, Kojima H, Fukui M (2022) Dissimilatory microbial sulfur and methane metabolism in the water column of a shallow meromictic lake. Syst Appl Microbiol 45:126320 PubMed Crossref
Weber L, Gonzalez-Díaz P, Armenteros M, Apprill A (2019) The coral ecosphere: a unique coral reef habitat that fosters coral-microbial interactions. Limnol Oceanogr 64:2373-2388 Crossref
Wolfe K, Kenyon TM, Mumby PJ (2021) The biology and ecology of coral rubble and implications for the future of coral reefs. Coral Reefs 40:1769-1806 Crossref
Xia J, Zhu W, Liu X, Ren Y and others (2022) The effect of two types of grid transplantation on coral growth and the in-situ ecological restoration in a fragmented reef of the South China Sea. Ecol Eng 177:106558 Crossref
Xue J, Liu Y, Shi K, Qiao Y and others (2022) Responses of seawater bacteria in the bioremediation process of petroleum contamination by immobilized bacteria. J Environ Chem Eng 10:107133 Crossref
Yi M, Zhang L, Qin C, Lu P, Bai H, Han X, Yuan S (2022) Temporal changes of microbial community structure and nitrogen cycling processes during the aerobic degradation of phenanthrene. Chemosphere 286:131709 PubMed Crossref
Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE and others (2016) Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun 7:11833 PubMed Crossref
Zhang Q, Zhu T, Wang Y, Yao S, An N, Xiao Q (2023) Effect of biochar and hyper-thermal inoculum addition on polycyclic aromatic hydrocarbon-degrading bacteria during composting. Clean Soil Air Water 51:2200114 Crossref
Zhang X, Cheng K, Qin Y, Li X and others (2024) Coral mucus promotes the carbon metabolic potency of microorganisms in the coral reef ecosystem. Limnol Oceanogr 69:2348-2363 Crossref
Zhao H, Zhang J, Yang H, Li Y and others (2024) Coral reefs at Qiziwan National Marine Park in 2023: spatial variability and their relationship with environmental factors. Front Mar Sci 11:1407803 Crossref
Zhao Y, Yang H, Storey KB, Chen M (2014) RNA-seq dependent transcriptional analysis unveils gene expression profile in the intestine of sea cucumber Apostichopus japonicus during aestivation. Comp Biochem Physiol D Genomics Proteomics 10:30-43 PubMed Crossref
Zheng Q, Lu J, Wang Y, Jiao N (2019) Genomic reconstructions and potential metabolic strategies of generalist and specialist heterotrophic bacteria associated with an estuary Synechococcus culture. FEMS Microbiol Ecol 95:fiz017 PubMed Crossref
Zhu W, Zhao H, Ke J, Zhang J and others (2024) Deciphering the environmental adaptation and functional trait of core and noncore bacterial communities in impacted coral reef seawater. Sci Total Environ 931:172897 PubMed Crossref
He Zhao (Co-author)
1742961937@qq.com
Jingzhao Ke (Co-author)
1539264110@qq.com
Junling Zhang (Co-author)
1910305975@qq.com
Pei Yang (Co-author)
2601005953@qq.com
Xiangbo Liu (Co-author)
466537551@qq.com
Wentao Zhu (Co-author)
2274430217@qq.com
Aimin Wang (Co-author)
aimwang@163.com
Xiubao Li (Corresponding Author)
xiubaoli@hainanu.edu.cn
Handling Editor:
Steven Lohrenz, New Bedford, Massachusetts, USA
Reviewers:
T. Yeemin and 2 anonymous referees
Acknowledgements:
This work was financially supported by the Major Science and Technology plan of Hainan Province (ZDYF2023SHFZ173), the Innovative Talent Foundation of Hainan Province (KJRC2023C39), and the National Natural Science Foundation of China (42161144006 or 3511/21, 42076108).