Microbial diagenesis of dissolved organic matter from the ocean's surface to abyssal depths: a case study in the Humboldt upwelling system

Abstract

Marine dissolved organic matter (DOM) represents one of Earth's largest dynamic carbon pools-comparable in scale to atmospheric CO₂. Primarily derived from phytoplankton production in the sunlit surface ocean, DOM serves as a key substrate for heterotrophic microbes that actively transform and recycle it. The portion remaining after microbial diagenesis contributes to the long-lived deep-sea reservoir of refractory dissolved organic carbon (RDOC) with turnover times up to millennia. DOC lability is an important trait determining microbial utilization as well as carbon storage time in the ocean and can be inferred from its chemical composition, particularly changes in individual amino acids (AAs). In this study, we examined dissolved (DOC) and particulate organic carbon (POC) distribution, composition and concentration of dissolved hydrolyzable AAs (DHAA), microbial community structure, and activity along depth profiles from the surface to the abyssopelagic zone (down to 5,000 m) in the Humboldt upwelling system off Chile-one of the ocean's most productive regions. Our results show a pronounced decrease in DOC concentration and lability, and in viral and prokaryotic abundance with depth. Below the mesopelagic zone, DOC displayed characteristics of RDOC: <42 μmol C L^-1, [DHAA-C]:[DOC] ~ 0.6%, and a glycine fraction of ~75 mol% DHAA. Bacterial biomass production and extracellular enzyme activities (EEA), however, were detectable below the mesopelagic zone and even at abyssal depths, albeit at very low rates. Cell-specific EEA and the proportion of high nucleic acid (HNA) cells increased with depth suggesting adaptation to an extremely low-substrate environment. We discuss microbial carbon turnover under varying assumptions of bacterial growth efficiency and conclude that microbial life in the bathy- and abyssopelagic zones of the Humboldt Current is likely sustained by the flux of sinking particulate organic matter.

Keywords: Humboldt upwelling system; amino acids; deep ocean; dissolved organic matter; microbial activity.

Figure 1

Overview of the three working areas in the Humboldt Current off Chile sampled during RV SONNE expedition HOMER (SO288). The gridded bathymetry map was obtained from http://www.gebco.net (General Bathymetric Chart of the Oceans, GEBCO 2024 Grid).

Figure 2

(a–f) Whole water column profiles of temperature (T, a), oxygen (O₂, b), chlorophyll a (Chl a, c), and the inorganic nutrients [nitrate (NO₃, d), phosphate (PO₄, e), and silicate (SiO₂, f)], for the three stations sampled in the Humboldt current off Chile during SO288. Symbols: black (area 1), red (area 2), green (area 3).

Figure 3

(a–c) Distribution of particulate organic matter in the water column off Chile. Particulate organic nitrogen (PON, a), particulate organic carbon (POC, b), and the molar ratio of POC: PON (C:N, c). Boxes here and in the following figures represent the interquartile ranges, the line within the box the median, and the whiskers extend to the minimum and maximum values within 1.5 times the interquartile range.

Figure 4

(a–f) Concentrations of dissolved organic carbon (DOC, a), the proportion of carbon contained in DHAA to DOC (DHAA:DOC, b), and the degradation index (DI, c) based on the DHAA distribution, as well as individual AAs that indicate microbial degradation of DOM, specifically glycine (Gly, d), GABA (e), and leucine (Leu, f) over depth for the three stations sampled during SO288.

Figure 5

(a–f) Flow cytometry-based prokaryotic cell counts (a), the ratio of high to low nucleic acid content prokaryotic cells (HNA:LNA, b), virus counts (c), bacterial biomass production (BBP, d) based on ³H-leucine incorporation, BBP per bacterial cell (e), and bacterial carbon demand (BCD, f).

Figure 6

(a–h) Extracellular enzymatic activity (EEA) of alkaline phosphatase (APase), β-glucosidase (BGase), leucine aminopeptidase (LPase), and β-N-acetyl-glucosaminidase (NAG) for bulk (a–d) and cell-specific (e–h) measurements.

Figure 7

Microbiome community composition derived from 16S miTAG analysis. Relative abundance of prokaryotes (phylum level) in each size fraction grouped into pelagic zones.