Community Interaction Co-limitation: Nutrient Limitation in a Marine Microbial Community Context

Abstract

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 B12) 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.

Mechanisms Underpinning the Net Removal Rates of Dissolved Organic Carbon in the Global Ocean

“…For example, experiments show that iron can be limiting for bacterial growth in the surface ocean (Church et al., 2000) and potentially in the mesopelagic (Baltar et al., 2018), although a global modeling study found it to be not the main limiting factor (Pham et al., 2022). Similarly, community‐aspects of co‐limitations have not been included here (Bannon et al., 2022). Global models intentionally generalize and simplify, and assessing such microbial community effects on global scales using Earth System Models is currently out of reach, because the huge diversity of compounds and microorganisms still poses a huge challenge to models, and heterotrophic microorganisms are usually not even included.…”

Nutrient colimitation is a quantitative, dynamic property of microbial populations

“…In nature, colimitation of clonal populations is also layered with community colimitation, for instance, when members of the community have different nutrient preferences [31, 32]. In this case, the starting conditions of the system are even less clear than for clonal populations, and supplementation experiments that scan a surface of nutrient concentrations in multiple dimensions provide a critical advantage for quantifying the extent of limitation and the number of limiting resources.…”

Cobalamin Co‐Limits Phytoplankton and Bacterial Biomass and Activity in Eastern Mediterranean Coastal Waters

“…Estimates suggest that co‐limitation of marine microbial populations is a common phenomenon (Browning et al., 2017), and may affect the food‐web dynamics, the organism's nutritional requirements, and species distribution (Bannon et al., 2022). Currently, it is very hard to study this issue experimentally, especially because we lack a detailed understanding of individual phytoplankton/bacteria's nutritional requirements, community dynamics etc.…”

“…Previous studies from the SEMS coast showed that phytoplankton are primarily N‐limited, while heterotrophic prokaryotes are limited by organic carbon substrates and/or orthophosphate (Rahav et al., 2016). Given that many marine microorganisms are vitamin B 12 auxotrophs (Bannon et al., 2022), and that the SEMS coast are often affected by external anthropogenic inputs containing N and P (Kress & Galil, 2016), we hypothesized that nutrients limitation of phytoplankton and heterotrophic bacteria may be shifted to B 12 . Moreover, similarly to dissolved inorganic nutrients (e.g., orthophosphate, nitrate) and chlorophyll‐ a , surface B 12 concentrations in the Mediterranean Sea decreases as going eastward towards more oligotrophic waters (Bonnet et al., 2013).…”