Microbial Competition in the Subpolar Southern Ocean: An Fe–C Co-limitation Experiment

Abstract

Iron (Fe) is a paradox in the modern ocean -it is central to many life-critical enzymes but is scarce across most surface waters. The high cellular demand and low bioavailability of Fe likely puts selective pressure on marine microorganisms. Previous observations suggest that heterotrophic bacteria are outcompeted by small diatoms for Fe supply in the subantarctic zone of Southern Ocean, thereby challenging the idea of heterotrophic bacteria being more competitive than phytoplankton in the access to this trace metal. To test this hypothesis, incubation experiments were carried out at the Southern Ocean Time Series site (March-April 2016). We investigated (a) whether dissolved organic carbon (DOC), dissolved Fe, or both limit the growth of heterotrophic bacteria and, (b) if the presence of potential competitors has consequences on the bacterial Fe acquisition. We observed a pronounced increase in both bulk and cell-specific bacterial production in response to single (+C) and combined (+Fe+C) additions, but no changes in these rates when only Fe was added (+Fe). Moreover, we found that +Fe+C additions promoted increases in cell-specific bacterial Fe uptake rates, and these increases were particularly pronounced (by 13-fold) when phytoplankton were excluded from the incubations. These results suggest that auto-and heterotrophs could compete for Fe when DOC limitation of bacterial growth is alleviated. Such interactions between primary producers and nutrient-recyclers are unexpected drivers for the duration and magnitude of phytoplankton blooms in the Southern Ocean.

Resource Colimitation Drives Competition Between Phytoplankton and Bacteria in the Southern Ocean

“…The low rates of primary production and large‐scale upwelling of deep water containing low dissolved organic carbon (DOC) concentrations lead to some of the lowest surface DOC concentrations in the global ocean (∼40–50 µM, Hansell et al., 2012). While low surface dissolved Fe and DOC is thought to restrict heterotrophic bacterial (hereafter bacteria) growth in the Southern Ocean (Church et al., 2000; Obernosterer et al., 2015), studies from Fe‐limited regions have demonstrated that bacteria may also be significant consumers of dissolved Fe and can exhibit greater cellular Fe quotas than phytoplankton (Boyd et al., 2012; Fourquez et al., 2015, 2020; Tortell et al., 1996, 1999). High bacterial Fe demand and uptake rates compared to phytoplankton suggest that bacteria could be significant competitors for dissolved Fe in the Southern Ocean (Fourquez et al., 2015, 2020; Mazzotta et al., 2020).…”

Exopolymeric Substances Control Microbial Community Structure and Function by Contributing to both C and Fe Nutrition in Fe-Limited Southern Ocean Provinces

“…In this region, the relationships between bacterial production, primary production, C and Fe availability are dynamic and closely intertwined. In the SO, C, and Fe have been reported as being co-limiting for heterotrophic bacteria [ 9 , 13 ], with fierce competition between phytoplankton and bacteria for Fe acquisition. Moreover, such complex relationships can be affected by DOC produced by phytoplankton, which may enhance nutrient availability and bacterial growth (e.g., [ 46 ]).…”

“…At the Drake Passage (Bio 1 and 3), PLP concentrations and biodiversity were significantly influenced by C amendments with the largest impact seen with EPS amendment (L 22 and L 6, ), leading to increased PLP abundances and a concomitant decrease in their diversity ( Figure 5 ). Hence, the addition of EPS served as a key driver for heterotrophic bacteria ( Figure 8 ), likely relieving C limitation (e.g., [ 9 ]) in a subset of heterotrophic bacterial populations enabling them to outcompete the other bacterial populations.…”

“…Iron (Fe) limits the primary productivity in most of this high-nutrient low-chlorophyll a (Chl a ) (HNLC) region [ 7 , 8 ]. Fe acts as a limiting resource for which heterotrophic bacteria and phytoplankton compete [ 9 ], while viruses as well as grazers contribute to the release of their intracellular Fe [ 10 , 11 , 12 ]. Whereas heterotrophic bacteria from the SO can be limited by either Fe or C [ 9 , 13 ], the controls on viral activity are less well understood.…”

“…Fe acts as a limiting resource for which heterotrophic bacteria and phytoplankton compete [ 9 ], while viruses as well as grazers contribute to the release of their intracellular Fe [ 10 , 11 , 12 ]. Whereas heterotrophic bacteria from the SO can be limited by either Fe or C [ 9 , 13 ], the controls on viral activity are less well understood. Biological activity acts as a critical linkage between the cycling of Fe and C in the ocean [ 6 , 7 , 14 ], however, few experimental field studies have attempted to explicitly link them with collected data in the field.…”