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Temperature Responses of Heterotrophic Bacteria in Co-Culture with a Red Sea Synechococcus Strain

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Temperature Responses of Heterotrophic Bacteria in Co-Culture with a Red Sea Synechococcus Strain Temperature Responses of Heterotrophic Bacteria in Co-culture With a Red Sea Synechococcus Strain Item Type Article Authors Labban, Abbrar; Palacio, Antonio S.; García, Francisca C.; Hadaidi, Ghaida A.; Ansari, Mohd Ikram; López-Urrutia, Ángel; Alonso-Sáez, Laura; Hong, Pei-Ying; Moran, Xose Anxelu G. Citation Labban, A., Palacio, A. S., García, F. C., Hadaidi, G., Ansari, M. I., López-Urrutia, Á., … Morán, X. A. G. (2021). Temperature Responses of Heterotrophic Bacteria in Co-culture With a Red Sea Synechococcus Strain. Frontiers in Microbiology, 12. doi:10.3389/fmicb.2021.612732 Eprint version Publisher's Version/PDF DOI 10.3389/fmicb.2021.612732 Publisher Frontiers Media SA Journal Frontiers in Microbiology Rights This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Download date 01/10/2021 21:10:52 Item License https://creativecommons.org/licenses/by/4.0/ Link to Item http://hdl.handle.net/10754/669159 fmicb-12-612732 May 4, 2021 Time: 23:46 # 1 ORIGINAL RESEARCH published: 10 May 2021 doi: 10.3389/fmicb.2021.612732 Temperature Responses of Heterotrophic Bacteria in Co-culture With a Red Sea Synechococcus Strain Abbrar Labban1,2, Antonio S. Palacio3, Francisca C. García4, Ghaida Hadaidi1, Mohd I. Ansari1, Ángel López-Urrutia5, Laura Alonso-Sáez3, Pei-Ying Hong2 and Xosé Anxelu G. Morán1,5* 1 Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia, 2 Water Desalination and Reuse Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia, 3 AZTI, Marine Research, Basque Research and Technology Alliance (BRTA), Sukarrieta, Spain, 4 Environment and Sustainability Institute, University of Exeter, Penryn, United Kingdom, 5 Centro Oceanográfico de Gijón/Xixón, Instituto Español de Oceanografía, Gijón, Spain Edited by: Gipsi Lima Mendez, Catholic University of Louvain, Interactions between autotrophic and heterotrophic bacteria are fundamental for marine Belgium biogeochemical cycling. How global warming will affect the dynamics of these essential Reviewed by: microbial players is not fully understood. The aims of this study were to identify Eric A. Webb, University of Southern California, the major groups of heterotrophic bacteria present in a Synechococcus culture United States originally isolated from the Red Sea and assess their joint responses to experimental Malin Olofsson, University of Georgia, United States warming within the metabolic ecology framework. A co-culture of Synechococcus sp. *Correspondence: RS9907 and their associated heterotrophic bacteria, after determining their taxonomic Xosé Anxelu G. Morán affiliation by 16S rRNA gene sequencing, was acclimated and maintained in the [email protected] lab at different temperatures (24–34◦C). The abundance and cellular properties of Specialty section: Synechococcus and the three dominant heterotrophic bacterial groups (pertaining This article was submitted to to the genera Paracoccus, Marinobacter, and Muricauda) were monitored by flow Aquatic Microbiology, cytometry. The activation energy of Synechococcus, which grew at 0.94–1.38 d−1, a section of the journal Frontiers in Microbiology was very similar (0.34 ± 0.02 eV) to the value hypothesized by the metabolic theory Received: 30 September 2020 of ecology (MTE) for autotrophs (0.32 eV), while the values of the three heterotrophic Accepted: 29 March 2021 bacteria ranged from 0.16 to 1.15 eV and were negatively correlated with their Published: 10 May 2021 corresponding specific growth rates (2.38–24.4 d−1). The corresponding carrying Citation: Labban A, Palacio AS, García FC, capacities did not always follow the inverse relationship with temperature predicted by Hadaidi G, Ansari MI, López-Urrutia Á, MTE, nor did we observe a consistent response of bacterial cell size and temperature. Alonso-Sáez L, Hong P-Y and Our results show that the responses to future ocean warming of autotrophic and Morán XAG (2021) Temperature Responses of Heterotrophic Bacteria heterotrophic bacteria in microbial consortia might not be well described by theoretical in Co-culture With a Red Sea universal rules. Synechococcus Strain. Front. Microbiol. 12:612732. Keywords: Synechococcus, heterotrophic bacteria, metabolic ecology, temperature, growth rate, cell size, doi: 10.3389/fmicb.2021.612732 Red Sea Frontiers in Microbiology| www.frontiersin.org 1 May 2021| Volume 12| Article 612732 fmicb-12-612732 May 4, 2021 Time: 23:46 # 2 Labban et al. Temperature Effects on Microbial Co-culture INTRODUTION bacterioplankton classes in the ocean (Du et al., 2006; Willis et al., 2019). Bacterioplankton play significant roles in carbon and nutrient Temperature plays a fundamental role in the physiology of cycling in the oceans (Azam et al., 1983; Jiao et al., 2010; microorganisms (Edwards and Richardson, 2004; Montoya and Kirchman, 2016). The interactions between autotrophic and Raffaelli, 2010). Increasing temperature can impact planktonic heterotrophic bacteria are essential in marine food webs (Azam microbes either directly by altering their metabolism (Sarmento and Malfatti, 2007; Buchan et al., 2014), especially in oligotrophic et al., 2010) and individual size (Daufresne et al., 2009; Morán tropical and subtropical regions. There, heterotrophic bacteria et al., 2010), or indirectly by shifting their distribution or consume dissolved organic matter (DOM) ultimately fixed through increased stratification resulting in reduced nutrient photosynthetically by cyanobacteria (mostly belonging to the inputs into the upper layers (Behrenfeld et al., 2006; Keeling genera Prochlorococcus and Synechococcus) and other small et al., 2010). Although warming will enhance metabolism in phytoplankton (Azam and Malfatti, 2007). In turn, heterotrophic nutrient-sufficient conditions, there is an upper temperature bacteria facilitate the growth of primary producers including limit that every organism can tolerate (Heinrich, 1977). cyanobacteria by supplying fundamental micronutrients Traditionally described using the Q10 coefficient (Eppley, 1972; including vitamins (Hayashi et al., 2011), amino acids (Christie- Chen and Laws, 2017), another way of approaching the Oleza et al., 2015b) or scavenging the reactive oxygen species role of temperature in microbial plankton is through the (ROS) such as hydrogen peroxide (H2O2) from the environment framework of Metabolic Theory of Ecology (MTE) (Brown (Morris et al., 2008, 2011), which can be formed photochemically et al., 2004). Metabolism is obviously the result of a myriad in the oceans as a result of the photooxidation of DOM (Moffett of biochemical reactions (Morowitz et al., 2000; Brown et al., and Zika, 1987; Moffett and Zajiriou, 1990). H2O2 can cause cell 2004), but some generalizations have been made. According to damage and death in the absence of protective enzymes such the MTE, the effect of temperature on metabolic rates such as catalase that can decompose it to water and oxygen (Imlay, as specific growth rates can be described by the activation 2003). Since Prochlorococcus lacks this enzyme (Morris et al., energy. For autotrophs, with metabolic rates essentially equaling 2011) and Synechococcus has shown a weak catalase activity the mean rate of photosynthetic reactions (Farquhar et al., (Pena and Bullerjahn, 1995), specific groups of heterotrophic 1980), an activation energy of ca. 0.32 eV is predicted (Allen bacteria, by acting as H2O2 scavengers, can help the growth of et al., 2005; López-Urrutia et al., 2006). For heterotrophs, both cyanobacteria. their metabolic rates approach the mean rate of respiration Synechococcus is an ancient and genetically diverse genus (del Giorgio and Duarte, 2002; López-Urrutia et al., 2006), (Scanlan et al., 2009), partly due to horizontal gene transfer resulting in an activation energy of ca. 0.65 eV (Gillooly events (Zhaxybayeva et al., 2006; Coutinho et al., 2016). et al., 2001). Another general ecological theory that has The cell size of Synechococcus usually varies between 0.8 gained recent attention in the marine environment is the so- and 1.2 mm (Mella-Flores et al., 2012) and its genome called temperature-size rule (TSR), which suggests an inverse size ranges between 2.2 and 2.9 Mb (Scanlan et al., 2009). relationship between ambient temperature and individual size Based on the pigment composition of phycobiliproteins in the (Atkinson, 1994; Atkinson and Sibly, 1997). Originally developed photosynthetic antenna, all Synechococcus cells are composed of for metazoans (Azevedo et al., 2002), the decrease in individual phycocyanin (PC), whereas some strains contain both PC and size as a function of temperature has also been documented phycoerythrin (PE) (Liu et al., 2014), resulting in differently for picophytoplankton (Morán et al., 2010) and heterotrophic colored strains, ranging from blue-green to pink-orange (Wood bacteria (Morán et al., 2015). et al., 1985; Six et al., 2007). A recent study suggests that marine Global warming is impacting the structure and function representatives traditionally known as Synechococcus are actually of marine ecosystems worldwide. Although tropical planktonic comprised by three distinct taxa,
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