Nematodes play key roles in marine ecosystem. Although oceans cover 71% of the Earth's surface, none of marine model nematode has been reported. Here, we constructed the first inbred line of free-living marine nematode Litoditis marina, sequenced and assembled its genome. Furthermore, we successfully applied CRISPR/Cas9 genome editing in L. marina.Comparative genomics revealed that immunity and oxygen regulation genes are expanded, which is probably central to its sediment adaptation. While L. marina exhibits massive gene contractions in NHRs, chemoreceptors, xenobiotics detoxification and core histones, which could explain the more defined marine environment. Our experiments showed that dozens of H4 genes in Caenorhabditis elegans might contribute to its adaptation to the complex terrestrial environments, while two H4 genes in L. marina are involved in salinity stress adaptation. Additionally, ninety-two conserved genes appear to be positively selected in L. marina, which may underpin its osmotic, neuronal and epigenetic changes in the sea. With short generation time, highly inbred lines, and genomic resources, our report brings L. marina a promising marine animal model, and a unique satellite marine model to the wellknown biomedical model nematode C. elegans. This study will underpin ongoing work on animal functional genomics, environmental adaptation and developmental evolution. 4 marine nematodes have had their genomes sequenced and analysed (International Helminth Genomes Consortium 2019; Smythe et al. 2019; Weinstein et al. 2019). Oceans cover 71% of the Earth's surface, and represents almost 99% of available habitat, which are a key element for the existence and evolution of life (Robert 1999; Peng et al. 2020). In marine sediments, free-living nematodes abound both in numbers and in local species diversity, comprising about 80% of the abundance of meiofauna (Heip et al. 1985; Danovaro et al. 2010; Nascimento et al. 2012), they play a key role in the benthic food web and ecosystem. However, the study of marine nematodes is largely limited to taxonomy and ecology (De Meester et al. 2016; Derycke et al. 2016). Molecular mechanisms underlying their evolution, development regulation and adaptation mechanisms are rarely reported, and none of marine model nematode has been reported. The bacterivorous marine nematode Litoditis marina (Bastian, 1865) Sudhaus, 2011, formerly known as Rhabditis marina or Pellioditis marina, is found widely distributed in the littoral zone of coasts and estuaries of European, American, African and Asian countries, and play an important role in these marine ecosystems (Tietjen et al. 1970; Kito 1981; Houthoofd et al. 2003; Derycke et al. 2016). In addition, the embryonic cell lineage of L. marina has been reported by Houthoofd et al. (2003). In comparison with C. elegans, the overall L. marina lineage homology is 95.5%, whereas the fate homology is only 76.4%, and most of the differences in fate homology concern nervous, epidermal, and pharyngeal tissues, suggesting that L. marina wil...

Acetylcholine signaling has been reported to play essential roles in animal metabolic regulation and disease affected by diets. However, the underlying mechanisms that how diets regulate animal physiology and health are not well understood. Here we found that the acetylcholine receptor gene eat-2 was expressed in most of the pharyngeal muscles, which is in accordance to our previous report that EAT-2 received synaptic signals not only from pharyngeal MC neurons. The expression of fatty acid synthesis genes was significantly increased in both eat-2 and tmc-1 fast-growth mutants on CeMM food environment, compared to the wild-type. Excitingly, dietary fatty acids such as 15-methyl-hexadecanoic acid (C17ISO), palmitic acid (PA, C16:0) and stearic acid (SA, C18:0) supplementation, significantly accelerated wild-type worm development on CeMM, indicating that the fatty acid synthesis reprogramming is an essential strategy for C. elegans to regulate its development and growth on CeMM diet. Furthermore, we found that fatty acid elongase gene elo-6 knock-out significantly attenuated eat-2 mutant’ fast growth, while overexpression of elo-6 could rescue the eat-2; elo-6 double mutant’ slow development, which suggested that elo-6 played a major role in the above metabolic remodeling. Taken together, our report indicates that diets regulate neuromuscular circuit and modulate C. elegans development via fatty acid metabolic reprogramming. As most of the key genes and metabolites found in this study are conserved in both invertebrate and vertebrate animals, we believed that our results might provide essential clues to the molecular mechanisms underlying interactions among animal nutrition sensation, metabolism reprogramming and developmental regulation.Significance StatementDiets and nutritional composition affect animal development and human health, however the underlying mechanisms remain elusive. We demonstrate that the acetylcholine receptor gene eat-2 is expressed in most of pharyngeal muscles, and the expression of fatty acid synthesis genes is significantly increased in both eat-2 and tmc-1 fast-growth mutants on the synthetic chemical defined CeMM food environment. Dietary supplementation of several fatty acids significantly speed up animal development. Furthermore, we demonstrate that the fatty acid elongase gene elo-6 knock-out attenuates eat-2 mutant’ fast growth, and overexpression of wild-type elo-6 promotes the eat-2; elo-6 double mutant’ slow development. Our findings describe that acetylcholine signaling coordinate nutrition sensation and developmental regulation through fatty acid metabolic remodeling.