Microbial dysbiosis precedes signs of sea star wasting disease in wild populations of Pycnopodia helianthoides

Abstract

Sea star wasting (SSW) disease, a massive and ongoing epidemic with unknown cause(s), has led to the rapid death and decimation of sea star populations with cascading ecological consequences. Changes in microbial community structure have been previously associated with SSW, however, it remains unknown if SSW-associated dysbiosis is a mechanism or artifact of disease progression, particularly in wild populations. Here, we compare the microbiomes of the sunflower sea star, Pycnopodia helianthoides, before (Naïve) and during (Exposed and Wasting) the initial outbreak in Southeast Alaska to identify changes and interactions in the microbial communities associated with sea star health and disease exposure. We found an increase in microbial diversity (both alpha and beta diversity) preceding signs of disease and an increase in abundance of facultative and obligate anaerobes (most notably Vibrio) in both Exposed (apparently healthy) and Wasting animals. Complementing these changes in microbial composition was the initial gain of metabolic functions upon disease exposure, and loss of function with signs of wasting. Using Bayesian network clustering, we found evidence of dysbiosis in the form of co-colonization of taxa appearing in large numbers among Exposed and Wasting individuals, in addition to the loss of communities associated with Naïve sea stars. These changes in community structure suggest a shared set of colonizing microbes that may be important in the initial stages of SSW. Together, these results provide several complementary perspectives in support of an early dysbiotic event preceding visible signs of SSW.

Sea stars resist wasting through active immune and collagen systems

“…As above, the genes in these modules perform functions related to immunity, collagen processes and cell adhesion, while the microbes were among those previously identified as associate with health status in SSW [33]. (iii) Considering animals that remained asymptomatic across the course of the study, we find stability and resilience in microbial community composition despite laboratory conditions including artificial seawater, in contrast with other laboratory studies of coral and horseshoe crabs [54,55], but consistent with the observations of a core microbiome for Pisaster ochraceus [56] and Pycnopodia helianthoides [57] in the field. Interestingly, all four studies, including the present study, find Spirochaetes to be the dominant microbes of asymptomatic stars for both P. ochraceus and P. helianthoides and across multiple geographical locations and tissues [33,56,57].…”

“…(iii) Considering animals that remained asymptomatic across the course of the study, we find stability and resilience in microbial community composition despite laboratory conditions including artificial seawater, in contrast with other laboratory studies of coral and horseshoe crabs [54,55], but consistent with the observations of a core microbiome for Pisaster ochraceus [56] and Pycnopodia helianthoides [57] in the field. Interestingly, all four studies, including the present study, find Spirochaetes to be the dominant microbes of asymptomatic stars for both P. ochraceus and P. helianthoides and across multiple geographical locations and tissues [33,56,57]. The microbiome resilience we observe through time in the laboratory could be related to resistance to SSW, though further investigations are needed.…”

“…Though tracking changes in gene expression and microbiome composition of individual sea stars in the wild is unfeasible, it is important to note that these results may be specific to our laboratory conditions and may not represent the changes occurring during wasting in the wild. However, a study comparing the microbiomes of field-sampled naive, exposed and wasting sunflower sea stars, Pycnopodia helianthoides , in lieu of longitudinal sampling of individuals, in Alaska when the panzootic first reached the area, reveals a proliferation of anaerobic microbes with exposure and further with wasting [ 57 ], further supporting the idea that low oxygen may play an important role in SSW [ 19 ].…”

Recent molecular techniques to strengthen ecological studies in echinoderms

“…Traditional methods used in microbiology, such as culture and microscopy, have provided evidence of the presence of bacteria within the gut microbiota of sea urchins. Many of these bacteria are associated with ecological interactions and metabolic processes (Marangon et al, 2023;McCracken et al, 2023;Temara et al, 1993). However, recent advancements in molecular sequencing techniques have emerged as powerful tools that are revolutionizing the characterization of microbiota in marine organisms (Hakim et al, 2016;Nelson et al, 2010;Petti et al, 2005;Rodríguez-Barreras et al, 2021).…”

“…For instance, recent study revealed the gut microbiota of sea cucumbers (Pagán-Jiménez et al, 2019), revealing distinct microbial profiles among different species of sea cucumbers, and suggesting the influence of host-specific factors in shaping the composition of the gut microbiota. Another study examined the gut microbiota of a sea star and found the existence of specific microbial taxa involved in nutrient metabolism and the breakdown of complex organic compounds, highlighting the symbiotic relationship between the host and its gut microbiota in the digestive processes of sea stars (McCracken et al, 2023). In another study conducted with four Caribbean sea urchins, authors found similar gut microbiotas among the species, but one of them (Lytechinus variegatus) displayed specific microbiota profiles (Rodríguez-Barreras et al, 2021) (Fig.…”