Microplankton life histories revealed by holographic microscopy and deep learning

Abstract

The marine microbial food web plays a central role in the global carbon cycle. However, our mechanistic understanding of the ocean is biased toward its larger constituents, while rates and biomass fluxes in the microbial food web are mainly inferred from indirect measurements and ensemble averages. Yet, resolution at the level of the individual microplankton is required to advance our understanding of the microbial food web. Here, we demonstrate that, by combining holographic microscopy with deep learning, we can follow microplanktons throughout their lifespan, continuously measuring their three-dimensional position and dry mass. The deep-learning algorithms circumvent the computationally intensive processing of holographic data and allow rapid measurements over extended time periods. This permits us to reliably estimate growth rates, both in terms of dry mass increase and cell divisions, as well as to measure trophic interactions between species such as predation events. The individual resolution provides information about selectivity, individual feeding rates, and handling times for individual microplanktons. The method is particularly useful to detail the rates and routes of organic matter transfer in micro-zooplankton, the most important and least known group of primary consumers in the oceans. Studying individual interactions in idealized small systems provides insights that help us understand microbial food webs and ultimately larger-scale processes. We exemplify this by detailed descriptions of micro-zooplankton feeding events, cell divisions, and long-term monitoring of single cells from division to division.