Microbe-driven elemental cycling enables microbial adaptation to deep-sea ferromanganese nodule sediment fields.

BACKGROUND: Ferromanganese nodule-bearing deep-sea sediments cover vast areas of the ocean floor, representing a distinctive habitat in the abyss. These sediments harbor unique conditions characterized by high iron concentration and low degradable nutrient levels, which pose challenges to the survival and growth of most microorganisms. While the microbial diversity in ferromanganese nodule-associated sediments has been surveyed several times, little is known about the functional capacities of the communities adapted to these unique habitats. RESULTS: Seven sediment samples collected adjacent to ferromanganese nodules from the Clarion-Clipperton Fracture Zone (CCFZ) in the eastern Pacific Ocean were subjected to metagenomic analysis. As a result, 179 high-quality metagenome-assembled genomes (MAGs) were reconstructed and assigned to 21 bacterial phyla and 1 archaeal phylum, with 88.8% of the MAGs remaining unclassified at the species level. The main mechanisms of resistance to heavy metals for microorganisms in sediments included oxidation (Mn), reduction (Cr and Hg), efflux (Pb), synergy of reduction and efflux (As), and synergy of oxidation and efflux (Cu). Iron, which had the highest content among all metallic elements, may occur mainly as Fe(III) that potentially functioned as an electron acceptor. We found that microorganisms with a diverse array of CAZymes did not exhibit higher community abundance. Instead, microorganisms mainly obtained energy from oxidation of metal (e.g., Mn(II)) and sulfur compounds using oxygen or nitrate as an electron acceptor. Chemolithoautotrophic organisms (Thaumarchaeota and Nitrospirota phyla) were found to be potential manganese oxidizers. The functional profile analysis of the dominant microorganisms further indicated that utilization of inorganic nutrients by redox reactions (rather than organic nutrient metabolism) is a major adaptive strategy used by microorganisms to support their survival in the ferromanganese nodule sediments. CONCLUSIONS: This study provides a comprehensive metagenomic analysis of microbes inhabiting metal-rich ferromanganese nodule sediments. Our results reveal extensive redundancy across taxa for pathways of metal resistance and transformation, the highly diverse mechanisms used by microbes to obtain nutrition, and their participation in various element cycles in these unique environments. Video Abstract.

Two new species of nematodes from shallow and deep-water sediments in the South China Sea.

Two new species of free-living marine nematodes from the South China Sea are described: Gomphionema setiforme sp. nov. from intertidal sediment and Paracomesoma longissimum sp. nov. from upper continental slope sediment. Gomphionema setiforme sp. nov. is characterized by the punctated cuticle without lateral differentiation and cuticular pores; short cephalic setiform sensilla; spiral amphideal fovea with 4 turns close to the anterior body extremity; large cuticularized buccal cavity with a massive dorsal tooth; pharynx with a large posterior bulb; short, curved spicules; knife-like gubernaculum without apophyses and 11 cup-shaped precloacal supplements. Paracomesoma longissimum sp. nov. is characterized by cuticle with transverse rows of fine punctuations without lateral differentiation; buccal cavity with three teeth; lateral outer labial setiform sensilla 1.5 times as long as the other four outer labial setiform sensilla; spiral amphideal fovea with 2.5 turns; spicules 350360 m long or 15.716 times cloacal body diameter; plate-like gubernaculum without apophyses and 2528 papilliform precloacal supplements.

Two new species of Paramphimonhystrella (Nematoda, Monhysterida, Xyalidae) from the deep-sea sediments in the Western Pacific Ocean and adjacent shelf seafloor.

Two new species of marine nematodes, Paramphimonhystrella longispicula sp. n. in the deep-sea sediments from the Philippine Sea in the tropical Western Pacific Ocean with the water depth of 3920-5176 m and P. eurystoma sp. n. in the shelf seafloor from the East China Sea with the water depth of 55-64 m, are described. Both species possess long and slender spicules, which are present only in the congener P. barbula, a species discovered from the continental slope of New Zealand. Paramphimonhystrella longispicula sp. n. can be easily distinguished from P. barbula by the relatively broader buccal cavity, the unequally long cervical setae and a higher number of terminal setae. Paramphimonhystrella eurystoma sp. n. is unique in having a peculiar gubernaculum with two proximal capitula and a peculiar hammer-shaped cuticularized piece posterior to vulva, by which it can be distinguished from P. longispicula sp. n. and P. barbula as well as other congeners. Paramphimonhystrella longispicula sp. n. differs from P. eurystoma sp. n. also by the number of terminal setae (4 vs. 2). A dichotomous key to nine valid species of Paramphimonhystrella is provided.

Four new species of Epacanthion Wieser, 1953 (Nematoda: Thoracostomopsidae) in intertidal sediments of the Nanji Islands from the East China Sea.

Four new species of Epacanthion are described from intertidal sandy sediments in the Nanji Islands National Marine Natural Reserve from the East China Sea. Males of all four new species have short spicules (< 2 anal body diameter) and a characteristic cervical circle of distinctly short and densely arranged setae at the pharyngeal region: Epacanthion hirsutum sp. nov. with a cervical circle of a single row of setae posterior to the nerve ring; E. longicaudatum sp. nov. with a cervical circle of 16 bundles each composed of six setae in two longitudinal rows posterior to the nerve ring; E. fasciculatum sp. nov. with a cervical circle of 18 bundles each composed of about 10 setae posterior to the nerve ring; and E. sparsisetae sp. nov. with a cervical circle of eight bundles each composed of about 10 setae anterior to the nerve ring. Among the known species of Epacanthion, only two species possess these features: E. quadridisci and E. gorgonocephalum. Epacanthion quadridiscus has six bundles of setae situated at the same level of the nerve ring, while E. gorgonocephalum has distinctly dense setae forming a wide band at the pharyngeal region. Epacanthion hirsutum sp. nov. differs from all congeners by the cervical circle composed of a single row of setae. Epacanthion sparsisetae sp. nov. is unique in having the cervical circle of bundles anterior to the nerve ring. Epacanthion longicaudatum sp. nov. differs from E. fasciculatum sp. nov. by the body size and the structure of the cervical circle. An updated diagnostic key to 28 valid species of Epacanthion is proposed.

Paroctonchus nanjiensis gen. nov., sp. nov. (Nematoda, Enoplida, Oncholaimidae) from intertidal sediments in the East China Sea.

Paroctonchus nanjiensis gen. nov., sp. nov. is described from a sand beach in the China Nanji Islands Natural Reserve in the East China Sea. Paroctonchus nanjiensis is distinct in the family Oncholaimidae in having more than three teeth, a character found otherwise only in the monotypic genera Octonchus and Patagonema. The new genus and species differs from Octonchus and Patagonema in the number and pattern of teeth, bearing three large teeth with the left ventrosublateral one the largest plus about 27 small teeth distributed on the wall of buccal cavity. By contrast, Octonchus possesses one large tooth plus eight small teeth, while Patagonema has three large teeth with the right ventrosublateral one the largest plus 12 small teeth on three mandibular ridges. Moreover, Paroctonchus nanjiensis differs from Octonchus also in position of the amphidial aperture (located in the middle portion of buccal cavity vs. at the base of buccal cavity), and from Patagonema in the absence of a demanian system (vs. present) and the presence of two subventral rows of wart-like precloacal supplements (vs. a ventral row of papillate supplements). We provide an improved diagnosis for the subfamily Octonchinae, and discuss the evolution of teeth in the family Oncholaimidae.