Temperature Stress Induces Shift from Co-Existence to Competition

ORIGINAL RESEARCH published: 11 February 2021 doi: 10.3389/fmicb.2021.607601 Temperature Stress Induces Shift From Co-Existence to Competition for Organic Carbon in Microalgae- Bacterial Photobioreactor Community – Enabling Continuous Production of Microalgal Biomass Eva Sörenson 1, Eric Capo 2, Hanna Farnelid 1, Elin Lindehoff 1 and Catherine Legrand 1* 1 Department of Biology and Environmental Science, Centre of Ecology and Evolution and Microbial Model Systems, Linnaeus University, Kalmar, Sweden, 2 Department of Chemistry, Umeå University, Umeå, Sweden To better predict the consequences of environmental change on aquatic microbial ecosystems it is important to understand what enables community resilience. The Edited by: mechanisms by which a microbial community maintain its overall function, for example, Jun Sun, Tianjin University of Science and the cycling of carbon, when exposed to a stressor, can be explored by considering three Technology, China concepts: biotic interactions, functional adaptations, and community structure. Interactions Reviewed by: between species are traditionally considered as, e.g., mutualistic, parasitic, or neutral but Claudia Coleine, University of Tuscia, Italy are here broadly defined as either coexistence or competition, while functions relate to Sarahi L. Garcia, their metabolism (e.g., autotrophy or heterotrophy) and roles in ecosystem functioning Stockholm University, Sweden (e.g., oxygen production, organic matter degradation). The term structure here align with *Correspondence: species richness and diversity, where a more diverse community is though to exhibit a Catherine Legrand [email protected] broader functional capacity than a less diverse community. These concepts have here been combined with ecological theories commonly used in resilience studies, i.e., adaptive Specialty section: This article was submitted to cycles, panarchy, and cross-scale resilience, that describe how the status and behavior Aquatic Microbiology, at one trophic level impact that of surrounding levels. This allows us to explore the resilience a section of the journal of a marine microbial community, cultivated in an outdoor photobioreactor, when exposed Frontiers in Microbiology to a naturally occurring seasonal stress. The culture was monitored for 6 weeks during Received: 17 September 2020 Accepted: 12 January 2021 which it was exposed to two different temperature regimes (21 ± 2 and 11 ± 1°C). Samples Published: 11 February 2021 were taken for metatranscriptomic analysis, in order to assess the regulation of carbon Citation: uptake and utilization, and for amplicon (18S and 16S rRNA gene) sequencing, to Sörenson E, Capo E, Farnelid H, Lindehoff E and Legrand C (2021) characterize the community structure of both autotrophs (dominated by the green Temperature Stress Induces Shift microalgae Mychonastes) and heterotrophs (associated bacterioplankton). Differential From Co-Existence to Competition gene expression analyses suggested that community function at warm temperatures was for Organic Carbon in Microalgae- Bacterial Photobioreactor based on concomitant utilization of inorganic and organic carbon assigned to autotrophs Community – Enabling Continuous and heterotrophs, while at colder temperatures, the uptake of organic carbon was Production of Microalgal Biomass. Front. Microbiol. 12:607601. performed primarily by autotrophs. Upon the shift from high to low temperature, community doi: 10.3389/fmicb.2021.607601 interactions shifted from coexistence to competition for organic carbon. Network analysis Frontiers in Microbiology | www.frontiersin.org 1 February 2021 | Volume 12 | Article 607601 Sörenson et al. Microalgal-Bacterial Interactions Enable Resilience indicated that the community structure showed opposite trends for autotrophs and heterotrophs in having either high or low diversity. Despite an abrupt change of temperature, the microbial community as a whole responded in a way that maintained the overall level of diversity and function within and across autotrophic and heterotrophic levels. This is in line with cross-scale resilience theory describing how ecosystems may balance functional overlaps within and functional redundancy between levels in order to be resilient to environmental change (such as temperature). Keywords: microalgae, bacteria, community, resilience, coexistence, competition, adaptive cycles, interactions INTRODUCTION ecosystems are commonly described through the presence or absence of the exchange of signals or metabolites, including Microorganisms make up ≈70% of the aquatic biomass and mutualistic, parasitic, or neutral relationships (Tipton et al., their interactions in the microbial loop are vital for the 2019). Here, the focus is on broad-scale community interactions, recycling of energy and nutrients that ensure the ecosystem disregarding any potential microalgal-bacterial cooperation services provided by aquatic food webs (Azam et al., 1983; apart from that that involves carbon. Broadly, the considered Bar-On et al., 2018). In addition, aquatic microorganisms interactions may primarily be characterized by either contribute ≈50% of the O2 in the atmosphere today (Field coexistence, governed by resource partitioning (Sörenson et al., et al., 1998; Behrenfeld et al., 2001). The impact of current 2020), or by competition for energy and nutrients, which and predicted environmental changes on aquatic may lead to competitive exclusion (Schoener, 1974; Chesson, microorganisms, including the increasing sea surface 2000). Both types of interactions influence biogeochemical temperatures (Collins and Knutti, 2013), is difficult to assess cycles, e.g., that of carbon, through potential functional changes due to the lack of studies using high-resolution molecular and variations in microbial community structure (Lindh and methods of microbial community interactions. The ability of Pinhassi, 2018; Sörenson et al., 2020). Functions relevant for aquatic microbial ecosystems to be resilient to disturbances, studies of aquatic microbial ecosystems commonly relate to on shorter or longer scales, depends on the interplay of whether organisms are autotrophs, heterotrophs, or mixotrophs, multiple factors (Allison and Martiny, 2008; Shade et al., which is defined by the type of carbon (inorganic, organic, 2012a). Identifying the behavior of key resilience mechanisms or both) they have the capacity to acquire as a food source in response to changed environmental conditions may lead and to use for energy production. Temporal dynamics in the to more accurate predictions of the effects of environmental structure of a community relate to its species richness or changes on biogeochemical cycles. Such knowledge could for diversity, in which a more diverse community is characterized instance enable the implementation of more locally adapted by a more efficient use of resources compared to a less diverse monitoring and management programs of aquatic microbial community that likely have a more narrow functional range ecosystems (Bernhardt and Leslie, 2013; Andersson et al., (Cardinale et al., 2006; Ptacnik et al., 2008). 2015). Several studies have suggested that the functional In resilience theory, the term panarchy has been used together capabilities of experimental microbial ecosystems, and thus with adaptive cycles and cross-scale resilience theories to describe their resilience, were not found to be related to the composition the sustainability of both social and ecological systems (Holling, of the communities (Fernandez et al., 2000; Wang et al., 1973; Peterson et al., 1998; Gunderson and Holling, 2002). 2011; Vanwonterghem et al., 2014; Louca and Doebeli, 2016), Adaptive cycles postulate four phases that a system continuously which might be explained by the large functional redundancy pass through: birth – growth and accumulation of resources and diversity that exists among microbial species (Louca et al., (r), maturation – conservation of established processes (K), 2017, 2018, 2020). Microbial ecosystems are complex and death – the release upon changed conditions (Ω), and renewal consist of several interacting levels, such as trophic levels, – the creative phase of reorganization and adaptation to new that enable the transfer of energy and nutrients within the conditions (α; Holling, 1973). Panarchy describes how separate microbial loop and further up in the food web. Adaptations levels within an ecosystem, each with their own adaptive cycle, to changed conditions seen at one level likely have an influence interact in order to accommodate and adapt to changed on the levels above or below (Gunderson and Holling, 2002). conditions. Where lower levels, primarily when entering the Thus, in order to gain a deeper understanding of the underlying Ω-phase, influence the level above (termed revolt) while the mechanisms of the resilience of microbial communities, it is upper levels, primarily during the K-phase, are able to buffer important to link experimental results with theories. In this the impact (termed remember), and thereby the levels together study, we focused on three interlinked mechanisms that affect the community resilience (Gunderson and Holling, 2002). together have the potential to influence microbial ecosystem Cross-scale resilience describes how ecosystems may become resilience in response to changed environmental conditions: resilient by balancing overlapping functional diversity within biotic interactions, functional adaptations, and community and functional redundancy across

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