Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter

Abstract

Background Microbiome in early life has long-term effects on the host’s immunological and physiological development and its disturbance is known to trigger various diseases in host Deuterostome animals. The sea cucumber Apostichopus japonicus is one of the most valuable marine Deuterostome invertebrates in Asia and a model animal in regeneration studies. To understand factors that impact on host development and holobiont maintenance, host-microbiome association has been actively studied in the last decade. However, we currently lack knowledge of early life core microbiome during its ontogenesis and how it benefits the host’s growth. Results We analyzed the microbial community in 28 sea cucumber samples from a laboratory breeding system, designed to replicate aquaculture environments, across six developmental stages (fertilized eggs to the juvenile stage) over a three years-period to examine the microbiomes’ dynamics and stability. Microbiome shifts occurred during sea cucumber larval ontogenesis in every case. Application of the most sophisticated core microbiome extraction methodology, a hybrid approach with abundance-occupancy core microbiome analyses (top 75% of total reads and > 70% occupation) and core index calculation, first revealed early life core microbiome consisted of Alteromonadaceae and Rhodobacteraceae, as well as a stage core microbiome consisting of pioneer core microbe Pseudoalteromonadaceae in A. japonicus, suggesting a stepwise establishment of microbiome related to ontogenesis and feeding behavior in A. japonicus. More interestingly, four ASVs affiliated to Alteromonadaceae and Rhodobacteraceae were extracted as early life core microbiome. One of the ASV (ASV0007) was affiliated to the Sulfitobactor strain BL28 (Rhodobacteraceae), isolated from blastula larvae in the 2019 raring batch. Unexpectedly, a bioassay revealed the BL28 strain retains a host growth-promoting ability. Further meta-pangenomics approach revealed the BL28 genome reads were abundant in the metagenomic sequence pool, in particular, in that of post-gut development in early life stages of A. japonicus. Conclusion Repeated rearing efforts of A. japonicus using laboratory aquaculture replicating aquaculture environments and hybrid core microbiome extraction approach first revealed particular ASVs affiliated to Alteromonadaceae and Rhodobacteraceae as the A. japonicus early life core microbiome. Further bioassay revealed the growth promoting ability to the host sea cucumber in one of the core microbes, the Sulfitobactor strain BL28 identified as ASV0007. Genome reads of the BL28 were abundant in post-gut development of A. japonicus, which makes us consider effective probiotic uses of those core microbiome for sea cucumber resource production and conservation. The study also emphasizes the importance of the core microbiome in influencing early life stages in marine invertebrates. Understanding these dynamics could offer pathways to improve growth, immunity, and disease resistance in marine invertebrates.

The interplay between host-specificity and habitat-filtering influences sea cucumber microbiota across an environmental gradient of pollution

“…Our study is likely to indicate the former, as we detected multiple dominant microbes with a beneficial role, such as Rhodobacteriaceae (keystone species in sea cucumber intestinal system, J. Yu et al, 2023; andRhizobiaceae (potentially aiding in pollutant breakdown, Teng et al, 2015) in sea cucumber within the highly polluted region. However, further studies are needed to test this hypothesis, disentangling the microbial contribution to the host's survival and tolerance to marine pollution.…”

Active Microbiota of Penaeus stylirostris Larvae: Partially Shaped via Vertical and Horizontal Transmissions and Larval Ontogeny

“…Vertical transmission of specific bacterial taxa from parents to their offspring has also been demonstrated in Rimicaris exoculta , a shrimp species living in hydrothermal vent areas [ 50 , 51 ], as well as in other marine hydrothermal or cold seep organisms such as clams [ 52 ] and aquatic macroorganisms such as fish or sponges [ 53 , 54 ]. Among the core microbiota, several lineages such as Alteromonas , Ascidiaceihabitans (formerly Roseobacter ), Halomonas , Litoricola , Leisingera , Micrococcus , Pseudoaltermonas , Rhodovulum , Ruegeria and Sulfitobacter might exhibit probiotic or beneficial activities [ 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 ]. Others have a putative antimicrobial activity or ixotrophic activity with evidence of ASV related to Aureispira or the OM27 Clade ( Bdellovibrionaceae, affiliated with the Bdellovibrio and like organisms) [ 6 , 65 ].…”