Bacteria and Archaea Regulate Particulate Organic Matter Export in Suspended and Sinking Marine Particle Fractions

Abstract

The biological carbon pump (BCP) in the Southern Ocean is driven by phytoplankton productivity and is a significant organic matter sink. However, the role of particle-attached (PA) and free-living (FL) prokaryotes (bacteria and archaea) and their diversity in influencing the efficiency of the BCP is still unclear. To investigate this, we analyzed the metagenomes linked to suspended and sinking marine particles from the Sub-Antarctic Southern Ocean Time Series (SOTS) by deploying a Marine Snow Catcher (MSC), obtaining suspended and sinking particulate material, determining organic carbon and nitrogen flux, and constructing metagenome-assembled genomes (MAGs). The suspended and sinking particle-pools were dominated by bacteria with the potential to degrade organic carbon. Bacterial communities associated with the sinking fraction had more genes related to the degradation of complex organic carbon than those in the suspended fraction. Archaea had the potential to drive nitrogen metabolism via nitrite and ammonia oxidation, altering organic nitrogen concentration. The data revealed several pathways for chemoautotrophy and the secretion of recalcitrant dissolved organic carbon (RDOC) from CO₂, with bacteria and archaea potentially sequestering particulate organic matter (POM) via the production of RDOC. These findings provide insights into the diversity and function of prokaryotes in suspended and sinking particles and their role in organic carbon/nitrogen export in the Southern Ocean. IMPORTANCE The biological carbon pump is crucial for the export of particulate organic matter in the ocean. Recent studies on marine microbes have shown the profound influence of bacteria and archaea as regulators of particulate organic matter export. Yet, despite the importance of the Southern Ocean as a carbon sink, we lack comparable insights regarding microbial contributions. This study provides the first insights regarding prokaryotic contributions to particulate organic matter export in the Southern Ocean. We reveal evidence that prokaryotic communities in suspended and sinking particle fractions harbor widespread genomic potential for mediating particulate organic matter export. The results substantially enhance our understanding of the role played by microorganisms in regulating particulate organic matter export in suspended and sinking marine fractions in the Southern Ocean.

Keywords: Marine Snow Catcher; Southern Ocean; carbon export; functional capacity; marine fractions; metagenomics; particulate organic matter; prokaryotes.

FIG 1

Marine Snow Catcher (MSC) deployment at Southern Ocean Time Series sites during the IN2019_V02 using RV Investigator collecting POC and PON from the suspended (SP) and sinking (SK) particle pool. (A) The sampling locations at the SOTS site stations 1 and 5 are slightly different in latitude and longitude (see Data Set S1, Tab 1). (B) POC concentrations for SP (light gray bars) and SK (dark gray bars); (C) PON concentration for SP and SK; (D) POC/PON ratio for SP and SK; (E) POC and PON export flux at five stations.

FIG 2

Taxonomic composition and distribution of the Southern Ocean Time Series prokaryotic communities, determined using single-copy marker genes (ribosomal protein genes) with the SingleM pipeline. (A) Venn diagram showing the core OTUs shared by suspended and sinking bacterial taxonomic composition; (B) Venn diagram showing the core OTU percentage of read abundance shared by suspended and sinking archaeal taxonomic composition; (C) heat map showing the percentages of abundance of the bacterial class composition in the suspended and sinking fractions at each station. Taxa with low abundance are colored blue, and those in higher abundance are white, while the highest are red. (D) Heat map showing the percentages of abundance of the archaeal class in the suspended and sinking communities at each station.

FIG 3

Predicted genes for both complex, central, and chemoautotrophic prokaryotic community from unbinned contigs based on the DRAM tool in both the suspended (SP) and sinking (SK) particle pool. The predicted genes are involved in chemoautotrophs (C1), carbon utilization (CU), carbohydrate active enzymes (CAZymes [CAZY]), hydrocarbon degradation (HD), nitrogen metabolism (N), photosynthesis (PS), and transporter systems (T). The color scale represents predicted gene counts, including gene copies. Detailed gene names and copies are given in Data Set S1: Tab 2 for bacteria and Tab 3 for archaea. (A) Bacterial community functional annotation; (B) archaeal community functional annotation.

FIG 4

Phylogenomic inference of our 24 MAGs. The phylogenomic tree was based on alignment of 40% of the marker gene present in our MAGs. (A) Bacterial MAGs (yellow) against Gammaproteobacteria (blue) and Cyanobacteria (orange); (B) archaeal MAGs (green) against Euryarchaeota (red) and Thaumarchaeota (purple).

FIG 5

Predicted and identified genes from the 24 MAGs involved in carbohydrate-active enzymes (CAZymes [CAZY]), hydrocarbon degradation (HD), nitrogen metabolism (N), and transporter systems (T) based on the DRAM pipeline. The color scale represents the gene counts/copies. (A) Bacterial functional annotation; (B) archaeal functional annotation.