The order Spirochaetales (Oren and Garrity, 2021), belonging to the class Spirochaetia of the phylum Spirochaetota, comprises a diverse group of pathogenic and non-pathogenic bacteria. This order has five families: Borreliaceae, Breznakiellaceae, Sphaerochaetaceae, Spirochaetaceae, Treponemataceae and “Termitinemataceae” (Brune et al., 2022, Song et al., 2021, Gupta et al., 2013). Members of Spirochaetaceae are either free-living or symbiotic, obligate or facultative anaerobes, mesophilic or thermophilic, and survive in hypersaline and alkaline conditions (Ben Hania et al., 2015, Dubinina et al., 2020, Sravanthi et al., 2016, Shivani et al., 2017). They are known to inhabit a wide range of ecological niches like arthropods, marine environments, and freshwaters (Graña-Miraglia et al., 2020, Ben Hania et al., 2015, Dubinina et al., 2020, Sravanthi et al., 2016, Shivani et al., 2017). Furthermore, only a few Spirochaetales, such as members belonging to the genera Alkalispirochaeta and Marispirochaeta, have been reported from India (Sravanthi et al., 2016, Shivani et al., 2017).

The majority of the Spirochaetales members were distinguished by their spiral morphology and the presence of endoflagella. However, non-motile and non-spiral members were also found, which are now classified in the family Sphaerochaetaceae (Bidzhieva et al., 2020) and include two validly published genera names: Pleomorphochaeta and Sphaerochaeta (Arroua et al., 2017, Bidzhieva et al., 2020). The 16S rRNA gene sequence-based phylogeny, along with biochemical and phenotypical analysis helped in designating Pleomorphochaeta, isolated from oil reservoirs and subseafloor, as a separate genus (Arroua et al., 2017, Arroua et al., 2018). However, the genome sequences of the species of Pleomorphochaeta are not available. Members of Spirochaetales have been found in many different microbiomes (De et al., 2020, Williams et al., 2022), including seaweeds (Tourneroche et al., 2020, Cifuentes et al., 2000). The phylum Spirochaetota does not have any species directly isolated from seagrasses or macroalgae.

Metagenomics, a cultivation-independent technique, facilitates the study of microbial communities, the identification of novel taxa, and the comprehension of their functional capabilities through the utilization of MAGs (metagenome-assembled genomes; Setubal, 2021). MAGs have been acknowledged as a valuable resource for the formulation of novel taxa (Palmer et al., 2022, Konstantinidis and Rosselló-Móra, 2015, Whitman, 2015, Whitman, 2016) and the code of nomenclature of prokaryotes (SeqCode), which permits DNA sequences as nomenclature types for organisms that cannot be reasonably maintained or deposited in culture collection centres (Hedlund et al., 2022, Whitman et al., 2022). The metagenomic insights from various regions helped in describing several novel taxa of members of the phylum Spirochaetota (Karnachuk et al., 2022, Shivani et al., 2017). The present study aims to uncover novel taxa within the Spirochaetales through the systematic examination of MAG sequences from algal and seagrass samples collected from the Gulf of Mannar, home to diverse marine microbial communities. Based on the combined 16S rRNA gene-based phylogeny, phylogenomic, comparative genomic, and metabolic pathway analysis of binned genomes JB008Ts, a new genus within the Spirochaetaceae family, Thalassospirochaeta gen. nov. is proposed. The binned genome JB007 also potentially belongs to a new genus, although it has not been named, as the genome does not meet the essential criteria for naming in SeqCode. The binned genome JB015 and its additional binned genomes (JB002, JB003, and JB004) belong to the same species and are closely related to the members belonging to the genus Pleomorphochaeta. However, their further taxonomic classification remains unresolved due to insufficient supporting evidence.