Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes

Changing tastes in marine microbe food webs Protists are single-celled organisms complete with nuclei, organelles, and symbionts, and possess a multiplicity of physiological talents. They are ubiquitous, abundant, and often neglected by science. Worden et al. review the challenges of understanding the role protists play in geochemical cycling in the oceans. These organisms can photosynthesize like plants, graze on bacteria and archaea, parasitize each other and bigger creatures, have sex, and sometimes do all these things serially as conditions change. Their activities may have a significant influence on carbon cycling, and research efforts need to be amplified to understand their functional importance in marine ecosystems. Science, this issue 10.1126/science.1257594 BACKGROUND Marine ecosystems are composed of a diverse array of life forms, the majority of which are unicellular—archaea, bacteria, and eukaryotes. The power of these microbes to process carbon, shape Earth’s atmosphere, and fuel marine food webs has been established over the past 40 years. The marine biosphere is responsible for approximately half of global primary production, rivaling that of land plants. Unicellular eukaryotes (protists) are major contributors to this ocean productivity. In addition to photosynthetic growth, protists exhibit a range of other trophic modes, including predation, mixotrophy (a combination of photosynthetic and predatory-based nutrition), parasitism, symbiosis, osmotrophy, and saprotrophy (wherein extracellular enzymes break down organic matter to smaller compounds that are then transported into the cell by osmotrophy). ADVANCES Sensitive field approaches have illuminated the enormous diversity of protistan life (much of it uncultured) and, coupled with activity measurements, are leading to hypotheses about their ecological roles. In parallel, large-scale sequencing projects are providing fundamental advances in knowledge of genome/gene composition, especially among photosynthetic lineages, many of which are complex amalgams derived from multiple endosymbiotic mergers. Marine protists have yielded insight into basic biology, evolution, and molecular machineries that control organismal responses to the environment. These studies reveal tightly controlled signaling and transcriptional regulation as well as responses to limitation of resources such as iron, nitrogen, and vitamins, and offer understanding of animal and plant evolution. With the formulation of better computational approaches, hypotheses about interactions and trophic exchanges are becoming more exact and modelers more assertive at integrating different data types. At the same time, the impacts of climate change are being reported in multiple systems, of which polar environments are the touchstone of change. OUTLOOK Driven by the need to translate the biology of cells into processes at global scales, researchers must bring the conceptual framework of systems biology into bigger “ecosystems biology” models that broadly capture the geochemical activities of interacting plankton networks. Existing data show that protists are major components of marine food webs, but deducing and quantifying their ecosystem linkages and the resulting influences on carbon cycling is difficult. Genome-based functional predictions are complicated by the importance of cellular structures and flexible behaviors in protists, which are inherently more difficult to infer than the biochemical pathways typically studied in prokaryotes. Alongside the plethora of genes of unknown function, manipulable genetic systems are rare for marine protists. The development of genetic systems and gene editing for diverse, ecologically important lineages, as well as innovative tools for preserving microbe-microbe interactions during sampling, for visual observation, and for quantifying biogeochemical transformations, are critical but attainable goals. These must be implemented in both field work and laboratory physiology studies that examine multiple environmental factors. Expanding genome functional predictions to identify the molecular underpinnings of protistan trophic modes and realistically constrain metabolism will position the field to build reliable cell systems biology models and link these to field studies. By factoring in true complexities, we can capture key elements of protistan interactions for assimilation into more predictive global carbon cycle models. Global biogeochemical and ecological models rely on understanding organismal biology and the interactions occurring in marine microbial food webs. Protists have multifarious roles from the sunlit surface ocean to leagues below. Understanding of protistan behaviors and adaptability lags far behind knowledge of evolutionary processes that have shaped their genomes. As such, microbial mediation of carbon fluxes and specific interactions remain ill-resolved and predictive capabilities are still weak. Strategies to narrow this gap involve iteration between experimental and observational field studies, controlled laboratory experiments, systems biology approaches that preserve cellular structures and behaviors using relevant model taxa, and computational approaches. The profound influence of marine plankton on the global carbon cycle has been recognized for decades, particularly for photosynthetic microbes that form the base of ocean food chains. However, a comprehensive model of the carbon cycle is challenged by unicellular eukaryotes (protists) having evolved complex behavioral strategies and organismal interactions that extend far beyond photosynthetic lifestyles. As is also true for multicellular eukaryotes, these strategies and their associated physiological changes are difficult to deduce from genome sequences or gene repertoires—a problem compounded by numerous unknown function proteins. Here, we explore protistan trophic modes in marine food webs and broader biogeochemical influences. We also evaluate approaches that could resolve their activities, link them to biotic and abiotic factors, and integrate them into an ecosystems biology framework.