The influence of microbial symbiotic state on sponge holobiont adaptability: from ecological strategies to climate responses

Global climate change is driving ocean warming and acidification, which are projected to have profound impacts on marine ecosystems, particularly benthic communities. Prolonged exposure to these stressors has resulted in a range of adverse effects, including disease outbreaks and mass mortality among invertebrates (e.g., bivalves and echinoderms), degradation of macroalgae and seagrass beds, and widespread coral bleaching and mortality. These events are altering the spatial structure and biodiversity of marine ecosystems. Sponges (Porifera), which are one of the earliest metazoans, are considered to possess greater adaptability to future ocean conditions than other benthic organisms such as corals. They are therefore predicted to emerge as potential “winners” under climate change. This resilience is largely attributed to their diverse and complex microbial symbionts, which exhibit high plasticity and enhance the host’s ability to cope with environmental variation. Sponges exhibit two distinct microbial symbiotic states: high-microbial abundance (HMA) and low-microbial abundance (LMA), which are associated with different life strategies. This review summarizes current knowledge on the response of sponges with different microbial symbiotic states to environmental and climate changes. The microbial abundance of HMA sponges is typically 2–4 orders of magnitude higher than that of LMA sponges. HMA sponges also harbor more complex and diverse microbial communities. Moreover, they differ significantly in terms of physiological structure and microbial community functions, reflecting their divergent nutritional patterns and ecological strategies. HMA sponges harbor microbial communities that are more diverse, specialized, stable, and interactive, forming a stable, “closed” system finely tuned to their environment. Conversely, LMA sponge-associated microorganisms employ a more flexible, “open” strategy, characterized by lower diversity and higher dynamical variability to cope with environmental changes. These differences in nutritional and environmental adaptation strategies between LMA and HMA sponges largely reflect the distinct evolutionary histories. The LMA phenotype is considered ancestral, whereas the HMA phenotype may have evolved multiple transformations from LMA ancestors under strong selection pressure for ecological specialization. HMA phenotype exhibits high host specificity and a significant phylosymbiosis signature. The superior chemical defense capabilities of HMA sponges compared to those of LMA sponges, likely provide a significant environmental adaptation advantage that facilitated the evolutionary transition from LMA to HMA holobiont. This advantage itself is also a product of reciprocal selection between the host and its microbial symbionts. Furthermore, these divergent ecological strategies may also shape their differential responses of HMA and LMA sponges to climate change. Although species-specific variations exist, preliminary evidence indicates that HMA sponges generally experience less adverse effects from ocean warming (OW) and acidification (OA) than LMA sponges, exhibiting higher survival rates, less tissue necrosis, and greater microbial stability. However, it is not ruled out that some HMA sponges may be sensitive to climate change due to species-specific differences. While most sponges tolerate OA—with some photosynthetic species potentially benefiting from elevated CO2—OW presents a more severe threat, frequently leading to bleaching and mortality. Importantly, the interactive effects of OW and OA are species-dependent: acidification may mitigate thermal stress in some photosynthetic sponges but exacerbate it in heterotrophic species. In summary, this review analyzes the adaptive strategies of sponge-associated microorganisms and examines how host-microbe co-evolution may shape sponge resilience under future ocean conditions. We explore the differentiated responses of HMA and LMA sponges to OW and OA, and investigate potential correlations between different microbial symbiotic states and global climate change. While current evidence indicates that sponges have the potential to adapt to future environments, understanding species-specific responses and tolerance mechanisms remains critical. Such insights will improve predictions of future benthic community structure and ecosystem reorganization.