Search

The simultaneous limitation of productivity by two or more nutrients, commonly referred to as nutrient co-limitation, affects microbial communities throughout the marine environment and is of profound importance because of its impacts on various biogeochemical cycles. Multiple types of co-limitation have been described, enabling distinctions based on the hypothesized mechanisms of co-limitation at a biochemical level. These definitions usually pertain to individuals and do not explicitly, or even implicitly, consider complex ecological dynamics found within a microbial community. However, limiting and co-limiting nutrients can be produced in situ by a subset of microbial community members, suggesting that interactions within communities can underpin co-limitation. To address this, we propose a new category of nutrient co-limitation, community interaction co-limitation (CIC). During CIC, one part of the community is limited by one nutrient, which results in the insufficient production or transformation of a biologically produced nutrient that is required by another part of the community, often primary producers. Using cobalamin (vitamin B 12 ) and nitrogen fixation as our models, we outline three different ways CIC can arise based on current literature and discuss CIC's role in biogeochemical cycles. Accounting for the inherent and complex roles microbial community interactions play in generating this type of co-limitation requires an expanded toolset - beyond the traditional approaches used to identify and study other types of co-limitation. We propose incorporating processes and theories well-known in microbial ecology and evolution to provide meaningful insight into the controls of community-based feedback loops and mechanisms that give rise to CIC in the environment. Finally, we highlight the data gaps that limit our understanding of CIC mechanisms and suggest methods to overcome these and further identify causes and consequences of CIC. By providing this framework for understanding and identifying CIC, we enable systematic examination of the impacts this co-limitation can have on current and future marine biogeochemical processes., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Bannon, Rapp and Bertrand.)

Six aerobic alkanotrophs (organism that can metabolize alkanes as their sole carbon source) isolated from deep-sea hydrothermal vents were characterized using the radical clock substrate norcarane to determine the metalloenzyme and reaction mechanism used to oxidize alkanes. The organisms studied were Alcanivorax sp. strains EPR7 and MAR14, Marinobacter sp. strain EPR21, Nocardioides sp. strains EPR26w, EPR28w, and Parvibaculum hydrocarbonoclasticum strain EPR92. Each organism was able to grow on n-alkanes as the sole carbon source and therefore must express genes encoding an alkane-oxidizing enzyme. Results from the oxidation of the radical-clock diagnostic substrate norcarane demonstrated that five of the six organisms (EPR7, MAR14, EPR21, EPR26w, and EPR28w) used an alkane hydroxylase functionally similar to AlkB to catalyze the oxidation of medium-chain alkanes, while the sixth organism (EPR92) used an alkane-oxidizing cytochrome P450 (CYP)-like protein to catalyze the oxidation. DNA sequencing indicated that EPR7 and EPR21 possess genes encoding AlkB proteins, while sequencing results from EPR92 confirmed the presence of a gene encoding CYP-like alkane hydroxylase, consistent with the results from the norcarane experiments.

While nitrogen availability is known to limit primary production in large parts of the ocean, vitamin starvation amongst eukaryotic phytoplankton is becoming increasingly recognized as an oceanographically relevant phenomenon. Cobalamin (B(12)) and thiamine (B(1)) auxotrophy are widespread throughout eukaryotic phytoplankton, with over 50% of cultured isolates requiring B(12) and 20% requiring B(1). The frequency of vitamin auxotrophy in harmful algal bloom species is even higher. Instances of colimitation between nitrogen and B vitamins have been observed in marine environments, and interactions between these nutrients have been shown to impact phytoplankton species composition. This review surveys available data, including relevant gene expression patterns, to evaluate the potential for interactive effects of nitrogen and vitamin B(12) and B(1) starvation in eukaryotic phytoplankton. B(12) plays essential roles in amino acid and one-carbon metabolism, while B(1) is important for primary carbohydrate and amino acid metabolism and likely useful as an anti-oxidant. Here we will focus on three potential metabolic interconnections between vitamin, nitrogen, and sulfur metabolism that may have ramifications for the role of vitamin and nitrogen scarcities in driving ocean productivity and species composition. These include: (1) B(12), B(1), and N starvation impacts on osmolyte and antioxidant production, (2) B(12) and B(1) starvation impacts on polyamine biosynthesis, and (3) influence of B(12) and B(1) starvation on the diatom urea cycle and amino acid recycling through impacts on the citric acid cycle. We evaluate evidence for these interconnections and identify oceanographic contexts in which each may impact rates of primary production and phytoplankton community composition. Major implications include that B(12) and B(1) deprivation may impair the ability of phytoplankton to recover from nitrogen starvation and that changes in vitamin and nitrogen availability may synergistically impact harmful algal bloom formation.

The Ross Sea is home to some of the largest phytoplankton blooms in the Southern Ocean. Primary production in this system has previously been shown to be iron limited in the summer and periodically iron and vitamin B(12) colimited. In this study, we examined trace metal limitation of biological activity in the Ross Sea in the austral spring and considered possible implications for vitamin B(12) nutrition. Bottle incubation experiments demonstrated that iron limited phytoplankton growth in the austral spring while B(12), cobalt, and zinc did not. This is the first demonstration of iron limitation in a Phaeocystis antarctica-dominated, early season Ross Sea phytoplankton community. The lack of B(12) limitation in this location is consistent with previous Ross Sea studies in the austral summer, wherein vitamin additions did not stimulate P. antarctica growth and B(12) was limiting only when bacterial abundance was low. Bottle incubation experiments and a bacterial regrowth experiment also revealed that iron addition directly enhanced bacterial growth. B(12) uptake measurements in natural water samples and in an iron fertilized bottle incubation demonstrated that bacteria serve not only as a source for vitamin B(12), but also as a significant sink, and that iron additions enhanced B(12) uptake rates in phytoplankton but not bacteria. Additionally, vitamin uptake rates did not become saturated upon the addition of up to 95 pM B(12). A rapid B(12) uptake rate was observed after 13 min, which then decreased to a slower constant uptake rate over the next 52 h. Results from this study highlight the importance of iron availability in limiting early season Ross Sea phytoplankton growth and suggest that rates of vitamin B(12) production and consumption may be impacted by iron availability.