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The capacity of marine sponges to cope with environmental changes is often attributed to the specific composition of their bacterial communities. In this study, we assessed the bacterial microbiome of two dominant sponges, Rhabdastrella globostellata (Rg) and Hyrtios erectus (He), living in the Bouraké lagoon (New Caledonia), where abiotic conditions daily fluctuate according to the tide. Sponge specimens, sediment and seawater samples were collected at 2–3 m depth. The bacterial communities were assessed using 16S rRNA metabarcoding, and variations between the two sponges were compared using PCA biplots. Chloroflexi was the dominant phyla in both He and Rg with an average relative abundance of 41.2% and 53.2%, respectively, while it was absent in sediment and seawater. Among the phylum Chloroflexi, SAR202 clade was dominant in both sponges, reaching an average relative abundance of 53.2% (He) and 78.7% (Rg). Principal component analysis (PCA) was used to identify the main variables driving the bacterial community structure in both sponges. The results indicated that the bacterial community structure in both sponges was strongly associated with Chloroflexi (70.9% of the phyla variance) and SAR202 clade (86.6% of the clade variance). The high relative abundance of the phylum Chloroflexi and the SAR202 clade observed in this study is the highest reported so far in the literature in marine sponges. Such a high relative abundance of these bacteria could suggest their involvement in the well-being of sponges in the extreme environmental conditions of Bouraké.

International audience; Sponges are a key component of coral reef ecosystems and play an important role in carbon and nutrient cycles. Many sponges are known to consume dissolved organic carbon and transform this into detritus, which moves through detrital food chains and eventually to higher trophic levels via what is known as the sponge loop. Despite the importance of this loop, little is known about how these cycles will be impacted by future environmental conditions. During two years (2018 and 2020), we measured the organic carbon, nutrient recycling, and photosynthetic activity of the massive HMA, photosymbiotic sponge Rhabdastrella globostellata at the natural laboratory of Bouraké in New Caledonia, where the physical and chemical composition of seawater regularly change according to the tide. We found that while sponges experienced acidification and low dissolved oxygen at low tide in both sampling years, a change in organic carbon recycling whereby sponges stopped producing detritus (i.e., the sponge loop) was only found when sponges also experienced higher temperature in 2020. Our findings provide new insights into how important trophic pathways may be affected by changing ocean conditions.

According to current experimental evidence, coral reefs could disappear within the century if CO2 emissions remain unabated. However, recent discoveries of diverse and high cover reefs that already thrive under extreme conditions seem to contradict these projections. Volcanic CO2 vents, semi-enclosed lagoons and mangrove estuaries are unique study sites where one or more ecologically relevant parameters for life in the oceans are close or even worse than currently projected for the year 2100. These natural analogues of future conditions hold new hope for the future of coral reefs and provide unique natural laboratories to explore how reef species could keep pace with climate change. To achieve this, it is essential to characterize their environment as a whole, and accurately consider all possible environmental factors that may differ from what is expected in the future and that may possibly alter the ecosystem response. In this study, we focus on the semi-enclosed lagoon of Bouraké (New Caledonia, SW Pacific Ocean) where a healthy reef ecosystem thrives in warm, acidified and deoxygenated water. We used a multi-scale approach to characterize the main physical-chemical parameters and mapped the benthic community composition (i.e., corals, sponges, and macroalgae). The data revealed that most physical and chemical parameters are regulated by the tide, strongly fluctuate 3 to 4 times a day, and are entirely predictable. The seawater pH and dissolved oxygen decrease during falling tide and reach extreme low values at low tide (7.2 pHT and 1.9 mg O2 L−1 at Bouraké, vs 7.9 pHT and 5.5 mg O2 L−1 at reference reefs). Dissolved oxygen, temperature, and pH fluctuates according to the tide of up to 4.91 mg O2 L−1, 6.50 °C, and 0.69 pHT units on a single day. Furthermore, the concentration of most of the chemical parameters was one- to 5-times higher at the Bouraké lagoon, particularly for organic and inorganic carbon and nitrogen, but also for some nutrients, notably silicates. Surprisingly, despite extreme environmental conditions and altered seawater chemical composition, our results reveal a diverse and high cover community of macroalgae, sponges and corals accounting for 28, 11 and 66 species, respectively. Both environmental variability and nutrient imbalance might contribute to their survival under such extreme environmental conditions. We describe the natural dynamics of the Bouraké ecosystem and its relevance as a natural laboratory to investigate the benthic organism’s adaptive responses to multiple stressors like future climate change conditions.