Shifting microbial communities in acidified seawaters: insights from polychaetes living in the CO₂ vent of Ischia, Italy

Abstract

Oceans’ absorption of human-related CO₂ emissions leads to a process called ocean acidification (OA), consisting of the decrease of the seawater pH with negative consequences for many marine organisms. In this study, we investigate the microbial community of two species of polychaetes found in naturally acidified CO₂ vents: the nereid Platynereis massiliensis complex and the syllid Syllis prolifera. Animals were collected in the CO₂ vents of Castello Aragonese (Gulf of Naples, Ischia, Italy) in three zones at decreasing pH. For the analysis of the microbiome, the V3-V4 hypervariable region of the 16S ribosomal RNA gene of 40 worm samples was sequenced on an Illumina MiSeq platform. No difference in the microbial alpha diversity of both species was highlighted. On the contrary, the microbial composition of worms collected in the site at normal pH was different from that of the individuals obtained from the sites at lower pH. This effect was evident also in samples from the site with a slight, but relevant, degree of acidification. Amplicon sequence variants showing a significant variation among the groups of samples collected from different pH zones were reported for both polychaetes, but no common trend of variation was observed. The present study deepens our knowledge about the composition of polychaete microbiome in marine naturally acidified sites. Our results stress the importance of future investigations about the connection between the variation of environmental and polychaete microbial communities induced by OA and about the effect of these variations on polychaete key biological and ecological traits.

Keywords

climate change / microbiome / ocean acidification / Platynereis massiliensis complex / Syllis prolifera

References

[1] Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.

[2] Arcadi E, Rizzo C, Calogero R et al. (2023). Microbial communities inhabiting shallow hydrothermal vents as sentinels of acidification processes. Frontiers in Microbiology 14, 1233893.

[3] Arnoldi I, Negri A, Soresinetti L et al. (2022). Assessing the distribution of invasive Asian mosquitoes in Northern Italy and modelling the potential spread of Aedes koreicus in Europe. Acta Tropica 232, 106536.

[4] Assié A, Leisch N, Meier DV et al. (2020). Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria). The ISME Journal 14, 104–122.

[5] Barreto MM, Ziegler M, Venn A et al. (2021). Effects of ocean acidification on resident and active microbial communities of Stylophora pistillata. Frontiers in Microbiology 12, 707674.

[6] Baselga A (2010). Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19, 134–143.

[7] Biagi E, Caroselli E, Barone M et al. (2020). Patterns in microbiome composition differ with ocean acidification in anatomic compartments of the Mediterranean coral Astroides calycularis living at CO₂ vents. Science of The Total Environment 724, 138048.

[8] Botté ES, Nielsen S, Abdul Wahab MA et al. (2019). Changes in the metabolic potential of the sponge microbiome under ocean acidification. Nature Communications 10, 4134.

[9] Bressan M, Chinellato A, Munari M et al. (2014). Does seawater acidification affect survival, growth and shell integrity in bivalve juveniles? Marine Environmental Research 99, 136–148.

[10] Caldeira K, Wickett ME (2003). Anthropogenic carbon and ocean pH. Nature 425, 6956.

[11] Caldeira K, Wickett ME (2005). Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research 110, C09S04.

[12] Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583.

[13] Calosi P, Rastrick S, Lombardi C, De Guzman HJ, Davidson L, Jahnke M (2013). Adaptation and acclimatization to ocean acidification in marine ectotherms: An in situ transplant experiment with polychaetes at a shallow CO₂ vent system. Philosophical Transactions of the Royal Society B 368, 20120444.

[14] Del Olmo I, Roma-Cavagliani J, Martín-Hervás MDR et al. (2024). Integrative taxonomy in Syllis prolifera (Annelida, Syllidae): From a unique cosmopolitan species to a complex of pseudocryptic species. Invertebrate Systematics 38, IS24004.

[15] Del Pasqua M, Gambi MC, Caricato R, Lionetto MG, Giangrande A (2019). Effects of short-term and long-term exposure to ocean acidification on carbonic anhydrase activity and morphometric characteristics in the invasive polychaete Branchiomma boholense (Annelida: Sabellidae): A case-study from a CO₂ vent system. Marine Environmental Research 144, 203–212.

[16] Dixon P (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930.

[17] Ferrari C (2010). Biodiversità: Dal Genoma al Paesaggio. Zanichelli, Modena, Italy.

[18] Figuerola B, Hancock AM, Bax N et al. (2021). A review and meta-analysis of potential impacts of ocean acidification on marine calcifiers from the Southern Ocean. Frontiers in Marine Science 8, 584445.

[19] Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.

[20] Foo SA, Byrne M, Ricevuto E, Gambi MC (2018). The carbon dioxide vents of Ischia, Italy, a natural system to assess impacts of ocean acidification on marine ecosystems: An overview of research and comparisons with other vent systems. Oceanographic and Marine Biology 56, 237–310.

[21] Gambi M, Musco L, Giangrande A, Badalamenti F, Micheli F, Kroeker K (2016). Distribution and functional traits of polychaetes in a CO₂ vent system: Winners and losers among closely related species. Marine Ecology Progress Series 550, 121–134.

[22] Gambi MC, Manzo M, Giangrande A, Massa-Gallucci A (2017). Pilot study on population features of Syllis prolifera (Annelida, Syllidae) in relation to ocean acidification. Biologia Marina Mediterranea 24, 114–115.

[23] Giangrande A, Licciano M, Musco L (2005). Polychaetes as environmental indicators revisited. Marine Pollution Bulletin 50, 1153–1162.

[24] González-Delgado S, Hernández JC (2018). The importance of natural acidified systems in the study of ocean acidification: What have we learned? Advances in Marine Biology 80, 57–99.

[25] Hentschel U, Usher KM, Taylor MW (2006). Marine sponges as microbial fermenters. FEMS Microbiology Ecology 55, 167–177.

[26] Hochstein R, Zhang Q, Sadowsky MJ et al. (2019). The deposit feeder Capitella teleta has a unique and relatively complex microbiome likely supporting its ability to degrade pollutants. Science of the Total Environment 670, 547–554.

[27] IPCC (2019). IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (Pörtner HO, Roberts DC, Masson-Delmotte V et al., eds.). Cambridge University Press, Cambridge, UK and New York, NY, USA, 755 p.

[28] Ji M, Williams TJ, Montgomery K et al. (2021). Candidatus Eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations. The ISME Journal 15, 2692–2707.

[29] Jumars PA, Dorgan KM, Lindsay SM (2015). Diet of worms emended: An update of polychaete feeding guilds. Annual Review of Marine Science 7, 497–520.

[30] Kandler NM, Abdul Wahab MA, Noonan SHC et al. (2018). In situ responses of the sponge microbiome to ocean acidification. FEMS Microbiology Ecology 94, https://doi.org/10.1093/femsec/fiy205

[31] Kong N, Han S, Fu Q, Yu Z, Wang L, Song L (2022). Impact of ocean acidification on the intestinal microflora of the Pacific oyster Crassostrea gigas. Aquaculture 546, 737365.

[32] Kroeker KJ, Kordas RL, Crim R et al. (2013). Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Global Change Biology 19, 1884–1896.

[33] Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011). Divergent ecosystem responses within a benthic marine community to ocean acidification. PNAS 108, 14515–14520.

[34] Larsson A (2014). AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics 30, 3276–3278.

[35] Lebrato M, Andersson AJ, Ries JB et al. (2016). Benthic marine calcifiers coexist with CaCO₃-undersaturated seawater worldwide. Global Biogeochemical Cycles 30, 1038–1053.

[36] Lin YT, Xu T, Ip JC et al. (2023). Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis. Zoological Research 44, 106–125.

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

[38] Lucey NM, Lombardi C, DeMarchi L, Schulze A, Gambi MC, Calosi P (2015). To brood or not to brood: Are marine invertebrates that protect their offspring more resilient to ocean acidification? Scientific Reports 5, 12009.

[39] McFall-Ngai M, Hadfield MG, Bosch TCG et al. (2013). Animals in a bacterial world, a new imperative for the life sciences. PNAS 110, 3229–3236.

[40] McMurdie PJ, Holmes S (2013). Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217.

[41] Meron D, Atias E, Iasur Kruh L et al. (2011). The impact of reduced pH on the microbial community of the coral Acropora eurystoma. The ISME Journal 5, 51–60.

[42] Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012). Changes in coral microbial communities in response to a natural pH gradient. The ISME Journal 6, 1775–1785.

[43] Mirasole A, Badalamenti F, Di Franco A, Gambi MC, Teixidó N (2021). Boosted fish abundance associated with Posidonia oceanica meadows in temperate shallow CO₂ vents. Science of the Total Environment 771, 145438.

[44] Morgan M, Anders S, Lawrence M, Aboyoun P, Pagès H, Gentleman R (2009). ShortRead: A bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25, 2607–2608.

[45] Morrow KM, Bourne DG, Humphrey C et al. (2015). Natural volcanic CO₂ seeps reveal future trajectories for host-microbial associations in corals and sponges. The ISME Journal 9, 894–908.

[46] Munari M, Chiarore A, Signorini SG et al. (2022). Surviving in a changing ocean. Tolerance to acidification might affect the susceptibility of polychaetes to chemical contamination. Marine Pollution Bulletin 181, 113857.

[47] Orr JC, Fabry VJ, Aumont O et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 7059.

[48] Padmavathi AR, Pandian SK (2014). Antibiofilm activity of biosurfactant producing coral associated bacteria isolated from Gulf of Mannar. Indian Journal of Microbiology 54, 376–382.

[49] Palladino G, Caroselli E, Tavella T et al. (2022). Metagenomic shifts in mucus, tissue and skeleton of the coral Balanophyllia europaea living along a natural CO₂ gradient. ISME Communications 2, 65.

[50] Palombo C, Chiarore A, Ciscato M et al. (2023). Thanks mum. Maternal effects in response to ocean acidification of sea urchin larvae at different ecologically relevant temperatures. Marine Pollution Bulletin 188, 114700.

[51] Priscilla L, Rajeev M, Pandian SK et al. (2022). Gut associated culturable bacterial community in intertidal polychaete worms (Annelida: Polychaeta), their characterization and implications in captive shrimp aquaculture. Regional Studies in Marine Science 52, 102274.

[52] Quast C, Pruesse E, Yilmaz P et al. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.

[53] Range P, Teodósio Chícharo M, Ben-Hamadou R et al. (2014). Impacts of CO₂-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Regional Environmental Change 14, 19–30.

[54] Raulf FF, Fabricius K, Uthicke S et al. (2015). Changes in microbial communities in coastal sediments along natural CO₂ gradients at a volcanic vent in Papua New Guinea. Environmental Microbiology 17, 3678–3691.

[55] Sayem SMA, Manzo E, Ciavatta L et al. (2011). Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microbial Cell Factories 10, 74.

[56] Scanes E, Parker LM, Seymour JR et al. (2021). Microbiome response differs among selected lines of Sydney rock oysters to ocean warming and acidification. Fems Microbiology Ecology 97, fiab099.

[57] Shankar C, Sathianeson S, Viju N, Punitha S (2015). Antibacterial and biofilm inhibitory activities of bacteria associated with polychaetes. Journal of Coastal Life Medicine 3, 495–502.

[58] Signorini S, Munari M, Cannavacciuolo A et al. (2023). Investigation of the molecular mechanisms which contribute to the survival of the Polychaete Platynereis spp. under ocean acidification conditions in the CO₂ vent system of Ischia Island (Italy). Frontiers in Marine Science 9, 1067900.

[59] Simonetti S, Zupo V, Gambi MC, Luckenbach T, Corsi I (2022). Unravelling cellular and molecular mechanisms of acid stress tolerance and resistance in marine species: New frontiers in the study of adaptation to ocean acidification. Marine Pollution Bulletin 185, 114365.

[60] Sunday JM, Fabricius KE, Kroeker KJ et al. (2017). Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nature Climate Change 7, 81–85.

[61] Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014). Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PLoS ONE 9, e105592.

[62] Tangherlini M, Corinaldesi C, Ape F et al. (2021). Ocean acidification induces changes in virus-host relationships in Mediterranean Benthic Ecosystems. Microorganisms 9, 769.

[63] Teixidó N, Carlot J, Alliouane S et al. (2024). Functional changes across marine habitats due to ocean acidification. Global Change Biology 30, e17105.

[64] Teixidó N, Gambi MC, Parravacini V et al. (2018). Functional biodiversity loss along natural CO₂ gradients. Nature Communications 9, 5149.

[65] Thomas TRA, Kavlekar DP, LokaBharathi PA (2010). Marine drugs from sponge-microbe association—A review. Marine Drugs 8, 1417–1468.

[66] Thukral A (2017). A review on measurement of Alpha diversity in biology. Agricultural Research Journal 54, 1–10.

[67] Valvassori G, Benedetti M, Regoli F, Gambi MC (2019). Antioxidant efficiency of Platynereis spp. (Annelida, Nereididae) under different pH conditions at a CO₂ vent's system. Journal of Marine Biology 2019, 8415916.

[68] Vijayan N, Lema KA, Nedved BT et al. (2019). Microbiomes of the polychaete Hydroides elegans (Polychaeta: Serpulidae) across its life-history stages. Marine Biology 166, 19.

[69] Villanueva RA, Chen Z (2019). ggplot2: Elegant graphics for data analysis (2nd ed.). Measurement: Interdisciplinary Research and Perspectives 17, 160–167.

[70] Webster NS, Negri AP, Botté ES (2016). Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Scientific Reports 6, 19324.

[71] Webster NS, Negri AP, Flores F et al. (2013). Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environmental Microbiology Reports 5, 243–251.

[72] Wäge J, Valvassori G, Hardege JD, Schulze A, Gambi MC (2017). The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: Are phylogeographic patterns related to exposure to ocean acidification? Marine Biology 164, 199.

RIGHTS & PERMISSIONS

2024 The Author(s). Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.