Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean

Abstract

SignificanceBiological dinitrogen (N2) fixation (BNF) is an important source of nitrogen in marine systems. Until recently, it was believed to be primarily limited to subtropical open oceans. Marine BNF is mainly attributed to cyanobacteria. However, recently an unusual N2-fixing unicellular cyanobacteria (UCYN-A)/haptophyte symbiosis was reported with a broader temperature range than other N2-fixing cyanobacteria. We report that the UCYN-A symbiosis is present and fixing N2 in the Western Arctic and Bering Seas, further north than any previously reported N2-fixing marine cyanobacteria. Nanoscale secondary ion mass spectrometry enabled us to directly show that the symbiosis was fixing N2. These results show that N2-fixing cyanobacteria are not constrained to subtropical waters and challenge commonly held ideas about global marine N2 fixation.

High Rates of N2 Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

“…Planktonic N 2 fixation rates by some marine cyanobacteria are thought to be limited by temperature (Carpenter & Capone, 2008). N 2 fixation by cyanobacteria was previously thought to be constrained to surface waters with temperatures >20°C (e.g., Carpenter & Capone, 2008), but more recently, active N 2 fixation has been detected in higher-latitude temperate regions (Cassar et al, 2018;Moisander et al, 2010) and even coastal Arctic Seas (Blais et al, 2012;Harding et al, 2018;Sipler et al, 2017). However, linear regression analyses suggest no relationship between water temperature and N 2 fixation rates either in the pooled data (R 2 = 0.10) or in surface waters (R 2 = 0.08).…”

“…Cyanobacterial diazotrophs may contribute to primary productivity directly Montoya et al, 2004) or participate in symbioses with other photoautotrophic phytoplankton (Carpenter et al, 1999;Foster et al, 2007;Harding et al, 2018), while heterotrophic diazotrophs may rely on primary producers for a supply of organic carbon (Moisander et al, 2012). Cyanobacterial diazotrophs may contribute to primary productivity directly Montoya et al, 2004) or participate in symbioses with other photoautotrophic phytoplankton (Carpenter et al, 1999;Foster et al, 2007;Harding et al, 2018), while heterotrophic diazotrophs may rely on primary producers for a supply of organic carbon (Moisander et al, 2012).…”

“…We now know that marine diazotrophs are diverse and include unicellular cyanobacteria as well as noncyanobacterial diazotrophs that occupy a wider range of marine habitats than previously thought (Berthelot et al, 2017;Bombar et al, 2016;Messer et al, 2016;Moisander et al, 2010;Rees et al, 2009;Zehr & Turner, 2001), but we know little about their physiological capabilities and environmental controls on their biogeography. High N 2 fixation rates have now been measured during summer in temperate northwestern Atlantic and Pacific coastal waters when dissolved N concentrations in surface water were seasonally depleted (Mulholland et al, 2012;Shiozaki et al, 2015), in temperate and tropical coastal systems (Cassar et al, 2018;Chen et al, 2014;Grosse et al, 2010;Larsson et al, 2001;Moisander et al, 2010;Mulholland et al, 2012;Rees et al, 2009;Shiozaki et al, 2015;Voss et al, 2006;Zhang et al, 2012), in nutrient-rich coastal upwelling systems (Voss et al, 2004;Wen et al, 2017), and in coastal Arctic Seas (Blais et al, 2012;Harding et al, 2018;Sipler et al, 2017), broadening the latitudinal range and the diversity of habitats supporting diazotrophy. Based on their phylogenetic affiliations and the lack of quantifiable N 2 fixation rates, the high nifH gene diversity and presence of diverse bacterial diazotroph groups in coastal systems were attributed to microorganisms being transported there from terrestrial systems or sediments, rather than to autochthonous populations of active planktonic diazotrophs (Jenkins et al, 2004;Zehr et al, 2003).…”

Machine Learning Estimates of Global Marine Nitrogen Fixation

“…This is in line with recent observations that suggest that N 2 fixation may not be confined to warm and nutrient‐poor waters (Blais et al, ; Shiozaki et al, ). UCYN‐A has recently been found in cold waters (Harding et al, ; Shiozaki et al, ), and N 2 fixation could provide as much as 3.5 Tg N/year to the Arctic Ocean (Sipler et al, ). Differences between model simulations may be attributed to the parameterization of the types of diazotrophs in the models.…”

Variations in Rates of Biological Production in the Beaufort Gyre as the Arctic Changes: Rates From 2011 to 2016

“…A similar process may be happening here-recent work showed prevalent submesoscale dynamics in the early fall in the Beaufort Gyre (Mensa et al, 2018). Additionally, some of the required nitrogen could be supplied by nitrogen fixation, a process that was recently reported to occur in the Arctic Ocean (Harding et al, 2018;Sipler et al, 2017) or by urea (Varela et al, 2013).…”