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Aquatic Microbial Ecology 79:1 Vol. 79: 1–12, 2017 AQUATIC MICROBIAL ECOLOGY Published online March 28 https://doi.org/10.3354/ame01811 Aquat Microb Ecol Contribution to AME Special 6 ‘SAME 14: progress and perspectives in aquatic microbial ecology’ OPENPEN ACCESSCCESS REVIEW Exploring the oceanic microeukaryotic interactome with metaomics approaches Anders K. Krabberød1, Marit F. M. Bjorbækmo1, Kamran Shalchian-Tabrizi1, Ramiro Logares2,1,* 1University of Oslo, Department of Biosciences, Section for Genetics and Evolutionary Biology (Evogene), Blindernv. 31, 0316 Oslo, Norway 2Institute of Marine Sciences (ICM), CSIC, Passeig Marítim de la Barceloneta, Barcelona, Spain ABSTRACT: Biological communities are systems composed of many interacting parts (species, populations or single cells) that in combination constitute the functional basis of the biosphere. Animal and plant ecologists have advanced substantially our understanding of ecological inter- actions. In contrast, our knowledge of ecological interaction in microbes is still rudimentary. This represents a major knowledge gap, as microbes are key players in almost all ecosystems, particu- larly in the oceans. Several studies still pool together widely different marine microbes into broad functional categories (e.g. grazers) and therefore overlook fine-grained species/population-spe- cific interactions. Increasing our understanding of ecological interactions is particularly needed for oceanic microeukaryotes, which include a large diversity of poorly understood symbiotic rela- tionships that range from mutualistic to parasitic. The reason for the current state of affairs is that determining ecological interactions between microbes has proven to be highly challenging. How- ever, recent technological developments in genomics and transcriptomics (metaomics for short), coupled with microfluidics and high-performance computing are making it increasingly feasible to determine ecological interactions at the microscale. Here, we present our views on how this field will advance thanks to the progress in metaomics approaches as well as potential avenues for future research. KEY WORDS: Microeukaryotes · Interactions · Single-cell genomics · Single-cell transcriptomics · High-throughput sequencing THE MICROBIAL OCEAN abundant photoautotrophic (Synechococcus and Pro - chlorococcus) and heterotrophic (SAR11) pico-sized Our collective awareness of the significance of mar- prokaryotic plankton as well as novel lineages of het- ine ecosystems has increased steadily during the last erotrophic picoeukaryotes (e.g. MALV and MAST), 40 yr, progressing in concert with the development of the recognition of the importance of Archaea in new technologies that have allowed us to dig deeper oceanic plankton, the realization that the majority of into the microbial world. A number of key events can marine microbes cannot be cultured, the discovery of be identified from this period, for example the formu- the rare biosphere and the key role of viruses in lation of the microbial-loop concept, the discovery of oceanic communities (Kirchman 2008). © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Aquat Microb Ecol 79: 1–12, 2017 Most of these findings were initiated by a revolu- expression patterns or metabolisms using standard tion that started ~25 yr ago with the introduction of techniques. Much less is known regarding Point 2: molecular methods to marine microbial ecology. interactions between microbial species or popula- This revolution has generated a wealth of new tions within ecosystems. Here, interactions may knowledge, and during the last 8 yr, it has gained refer to classic ecological interactions (e.g. competi- renewed momentum with the advent of high- tion) (Box 1), structural interactions (e.g. one throughput sequencing platforms (Logares et al. microbe providing physical support for another) as 2012, Goodwin et al. 2016) and a variety of other well as metabolic interactions among organisms high-performance approaches such as genomics, (e.g. metabolic cooperation) (Raes & Bork 2008). transcriptomics, me tagenomics, metatranscriptom - Ecological interactions between microbes can be ics, proteomics and single-cell genomics (meta- negative (antagonistic), positive (synergistic) or neu- nomics for short). High-throughput sequencing has tral for the species involved (Lidicker 1979, Lead- been a key addition to the molecular toolbox of better & Poindexter 1986, Faust & Raes 2012) (Fig. 1, microbial ecologists, allowing a deeper exploration Box 1). of microbial diversity, dis tributions and metabolic Although these definitions are widely used for cat- functions. Questions that were impenetrable a egorizing organism’s life modes, the boundaries be- decade ago are now being addressed, such as the tween them in real-life can be blurred, as in para- magnitude of microbial diversity and its spatio - sitism vs. mutualism (Box 1) (Stat et al. 2008). temporal patterns (Sogin et al. 2006, Galand et al. Symbiosis (sensu lato) (Box 1) may be very common 2009, Pedrós-Alió 2012, Logares et al. 2013, 2014a, in marine planktonic protists (López-García & Mor- 2015, Rinke et al. 2013, Locey & Lennon 2016, eira 2008), and the character of the relationship be - Schloss et al. 2016). In addition, the introduction of tween host and symbiont can change not only in the high-performance metaomics techniques and the course of evolution but also during the host’s lifetime generation of big data is encouraging microbiolo- (Wagner-Döbler et al. 2010). Competition is the clas- gists to embark upon challenging studies which sic example where both species involved are nega- aim to understand the functioning of increasingly tively impacted by the interaction, while mutualism complex eco-systems. is its counterpart, bringing benefits for both. Para- sitism and predation represent typical examples of win-loss interactions, where one of the symbionts MOVING TOWARD OCEANIC gets all the benefits and the other assumes all the ECO-SYSTEMS BIOLOGY costs (Fig. 1, Box 1). Commensalism and amensalism are opposites too, with commensalism bringing ben- Despite the overall progress, there is a long road efits to one species at no cost for the other, while in ahead when moving from simplistic to holistic mod- amensalism, one of the interacting species is nega- els of oceanic ecosystem functioning. Such a sys- tively impacted by another with no benefits to itself tems biology approach, which aims at understand- (Fig. 1). Microbial interactions may require physical ing ecosystems as a whole by considering all contact between the cells involved (e.g. symbiosis) or molecular and ecological interactions that ultimately not. Within microbial communities, interactions that contribute to its functioning and which constitute do not require physical contact can be important for the interactome, is fundamental for our understand- instance when species release secondary metabolites ing of the global ocean as a large integrated system that inhibit the growth of other taxa (negative that regulate important parameters in the biosphere. allelopathy) (Legrand et al. 2003) or when released To achieve such holistic understanding, at least 2 metabolic by-products turn out to be essential for types of ecosystem data are needed: (1) a list of other members of the community (e.g. vitamins) components, represented by species or populations, (Sañudo-Wilhelmy et al. 2014). Although several and (2) the interactions between these components experiments and field studies have investigated in a spatiotemporal context (Raes & Bork 2008). In microbial intra-/inter-specific competition (Fredrick- microbes, the use of metanomics has contributed son & Stephanopoulos 1981), predation (Guerrero et substantially to increase our understanding of Point al. 1986, Berney et al. 2013), parasitism (Chambouvet 1: species or population diversity within communi- et al. 2008), mutualism/symbiosis (Gast & Caron ties. Still, most microbial species remain unknown 1996), and detritivory (Kirchman 2008), the majority or poorly known because they are currently uncul- of interactions among marine microbes is still un- turable, limiting our access to their genomes, gene- known. Krabberød et al.: Interactions in marine microeukaryotes 3 Box 1. Ecological interactions from a microbial perspective Symbiosis in its broadest sense refers to 2 biologically different species living together in a close and long-term relation- ship (de Bary 1879, Wilkinson 2001, Martin & Schwab 2013). Different types of symbiotic relationships are commonly cat- egorized into overlapping categories ranging from those that are harmful for one or both of the partners (i.e. competition and parasitism) to those where both partners benefit from the interaction (e.g. mutualism; Fig. 1). Holobiont refers to a host and all its symbiotic partners (Margulis & Fester 1991). A classic example of a holobiont would be a coral reef, which consists not only of the host and the dinoflagellate photosymbionts but also of marine fungi and other microorganisms (Amend et al. 2012, del Campo et al. 2016). Mutualism is a symbiotic relationship in which both partners benefit from the association. The degree to which the sym- bionts in the mutualistic relationship depend on each other can range from short-term interactions to obligatory symbiosis where
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