Marine macroalgae produce abundant and diverse polysaccharides, which contribute substantially to the organic matter exported to the deep ocean. Microbial degradation of these polysaccharides plays an important role in the turnover of macroalgal biomass. Various members of the Planctomycetes-Verrucomicrobia-Chlamydia (PVC) superphylum are degraders of polysaccharides in widespread anoxic environments. In this study, we isolated a novel anaerobic bacterial strain NLcol2T from microbial mats on the surface of marine sediments offshore Santa Barbara, CA, USA. Based on 16S ribosomal RNA (rRNA) gene and phylogenomic analyses, strain NLcol2T represents a novel species within the Pontiella genus in the Kiritimatiellota phylum (within the PVC superphylum). Strain NLcol2T is able to utilize various monosaccharides, disaccharides, and macroalgal polysaccharides such as agar and ɩ-carrageenan. A near-complete genome also revealed an extensive metabolic capacity for anaerobic degradation of sulfated polysaccharides, as evidenced by 202 carbohydrate-active enzymes (CAZymes) and 165 sulfatases. Additionally, its ability of nitrogen fixation was confirmed by nitrogenase activity detected during growth on nitrogen-free medium, and the presence of nitrogenases (nifDKH) encoded in the genome. Based on the physiological and genomic analyses, this strain represents a new species of bacteria that may play an important role in the degradation of macroalgal polysaccharides and with relevance to the biogeochemical cycling of carbon, sulfur, and nitrogen in marine environments. Strain NLcol2T (= DSM 113125T = MCCC 1K08672T) is proposed to be the type strain of a novel species in the Pontiella genus, and the name Pontiella agarivorans sp. nov. is proposed.IMPORTANCEGrowth and intentional burial of marine macroalgae is being considered as a carbon dioxide reduction strategy but elicits concerns as to the fate and impacts of this macroalgal carbon in the ocean. Diverse heterotrophic microbial communities in the ocean specialize in these complex polymers such as carrageenan and fucoidan, for example, members of the Kiritimatiellota phylum. However, only four type strains within the phylum have been cultivated and characterized to date, and there is limited knowledge about the metabolic capabilities and functional roles of related organisms in the environment. The new isolate strain NLcol2T expands the known substrate range of this phylum and further reveals the ability to fix nitrogen during anaerobic growth on macroalgal polysaccharides, thereby informing the issue of macroalgal carbon disposal.

Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporation of DOM compounds into biomass is important to understand microbial niche partitioning. We conducted a series of DNA-stable isotope probing (SIP) experiments using 13C-labeled substrates of varying lability including amino acids, cyanobacteria lysate, and DOM from diatom and cyanobacteria isolates concentrated on solid phase extraction PPL columns (SPE-DOM). Amendments of substrates into Sargasso Sea bacterioplankton communities were conducted to explore microbial response and DNA-SIP was used to determine which lineages of Bacteria and Archaea were responsible for uptake and incorporation. Greater increases in bacterioplankton abundance and DOC removal were observed in incubations amended with cyanobacteria-derived lysate and amino acids compared to the SPE-DOM, suggesting that the latter retained proportionally more recalcitrant DOM compounds. DOM across a range of bioavailability was utilized by diverse prokaryotic taxa with copiotrophs becoming the most abundant 13C-incorporating taxa in the amino acid treatment and oligotrophs becoming the most abundant 13C-incorporating taxa in SPE-DOM treatments. The lineages that responded to SPE-DOM amendments were also prevalent in the mesopelagic of the Sargasso Sea, suggesting that PPL extraction of phytoplankton-derived DOM isolates compounds of ecological relevance to oligotrophic heterotrophic bacterioplankton. Our study indicates that DOM quality is an important factor controlling the diversity of the microbial community response, providing insights into the roles of different bacterioplankton in resource exploitation and efficiency of marine carbon cycling.