Various morphotypes of large filamentous bacteria were isolated through micromanipulation from sulphidic sediment mats in the Bay of Concepción, central Chile. This study employed DNA amplification, whole-genome sequencing and bioinformatics analyses to unveil the taxonomic and genomic features of previously unidentified bacteria. The results revealed several novel genera, families and species, including three specimens belonging to Beggiatoales (Beggiatoaceae family), five to Desulfobacterales (Desulfobacteraceae family), two to the Chloroflexi phylum and one to the phylum Firmicutes. Metabolically, Beggiatoaceae bacteria exhibit a flexible and versatile genomic repertoire, enabling them to adapt to variable conditions at the sediment–water interface. All the bacteria demonstrated a mixotrophic mode, gaining energy from both inorganic and organic carbon sources. Except for the Firmicutes bacterium, all others displayed the ability to grow chemolithoautotrophically using H₂ and CO₂. Remarkably, the reverse tricarboxylic acid (rTCA) and Calvin–Benson–Bassham (CBB) pathways coexisted in one Beggiatoaceae bacterium. Additionally, various defence systems, such as CRISPR-Cas, along with evidence of viral interactions, have been identified. These defence mechanisms suggest that large filamentous bacteria inhabiting sulphidic sediments frequently encounter bacteriophages. Thus, robust defence mechanisms coupled with multicellularity may determine the survival or death of these large bacteria.