Biogeography of Cyanobacterial isiA Genes and Their Link to Iron Availability in the Ocean.

Qian Li,Nianzhi Jiao,Jef Huisman,Thomas S Bibby

doi:10.3389/fmicb.2019.00650

Abstract

The cyanobacterial iron-stress-inducible isiA gene encodes a chlorophyll-binding protein that provides flexibility in photosynthetic strategy enabling cells to acclimate to low iron availability. Here, we report on the diversity and abundance of isiA genes from 14 oceanic stations encompassing large natural gradients in iron availability. Synechococcus CRD1 and CRD2-like isiA genes were ubiquitously identified from tropical and subtropical waters of the Pacific, Atlantic, and Indian Oceans. The relative abundance of isiA-containing Synechococcus cells ranged from less than 10% of the total Synechococcus population in regions where iron is replete such as the North Atlantic subtropical gyre, to over 80% in low-iron but high-nitrate regions of the eastern equatorial Pacific. Interestingly, Synechococcus populations in regions with both low iron and low nitrate concentrations such as the subtropical gyres in the North Pacific and South Atlantic had a low relative abundance of the isiA gene. Indeed, fitting our data into a multiple regression model showed that ∼80% of the variation in isiA relative abundances can be explained by nitrate and iron concentrations, whereas no other environmental variables (temperature, salinity, Chl a) had a significant effect. Hence, isiA has a predictable biogeographical distribution, consistent with the perceived biological role of IsiA as an adaptation to low-iron conditions. Understanding such photosynthetic strategies is critical to our ability to accurately estimate primary production and map nutrient limitation on global scales.

Highlights

Picocyanobacteria belonging to the Synechococcus genus are among the most abundant photosynthetic organisms in open ocean ecosystems (Partensky et al, 1999; Scanlan and West, 2002) and are among the key contributors of primary production (Liu et al, 1998; Flombaum et al, 2013) and carbon cycling (Guidi et al, 2016)
IsiA gene diversity and abundance was retrieved from several oceanic environments, including samples from the equatorial Pacific Ocean (EEP1, EEP2, WPWP), equatorial Atlantic Ocean (At17), Northern Indian Ocean (NIO), Southern Indian Ocean (SIO), South China Sea (SCS), and Bering Sea (BS23, BS24) (Table 1 and Figure 1)
The high relative abundance of the isiA-containing Synechococcus (isiA) gene that we found in high-nutrient low-chlorophyll (HNLC) regions is in agreement with the distinct fluorescence signatures reported from these HNLC regions, which have commonly been attributed to the accumulation of chlorophyll-binding proteins such as IsiA (Behrenfeld et al, 2006, 2009; Schrader et al, 2011; Behrenfeld and Milligan, 2013; Macey et al, 2014)

Summary

Introduction

Picocyanobacteria belonging to the Synechococcus genus are among the most abundant photosynthetic organisms in open ocean ecosystems (Partensky et al, 1999; Scanlan and West, 2002) and are among the key contributors of primary production (Liu et al, 1998; Flombaum et al, 2013) and carbon cycling (Guidi et al, 2016). Biogeography of Cyanobacterial isiA Genes versatility of light-harvesting systems in the Synechococcus genus has substantially contributed to their ability to adapt to different underwater light environments (Stomp et al, 2004; Six et al, 2007) and exploit different ecological niches (Ting et al, 2002; Scanlan et al, 2009; Grébert et al, 2018) Their ability to change photosynthetic strategy in response to variation in iron availability (Bibby et al, 2001) is of particular interest as iron limits marine primary production in large oceanographic regions (Martin and Fitzwater, 1988; Behrenfeld et al, 1996; Boyd et al, 2000). IsiA may be expressed under other growth conditions, including high salt (Vinnemeier et al, 1998), high heat (Vinnemeier et al, 1998; Kojima et al, 2006) and high light (Havaux et al, 2005), acclimation to iron stress appears to be the primary functional role for this chlorophyll binding complex (Ghassemian and Straus, 1996; Bibby et al, 2001; Ryan-Keogh et al, 2012)

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