Transcriptional patterns identify resource controls on the diazotrophTrichodesmiumin the Atlantic and Pacific oceans

Abstract

The N-fixing cyanobacterium Trichodesmium is intensely studied because of the control this organism exerts over the cycling of carbon and nitrogen in the low nutrient ocean gyres. Although iron (Fe) and phosphorus (P) bioavailability are thought to be major drivers of Trichodesmium distributions and activities, identifying resource controls on Trichodesmium is challenging, as Fe and P are often organically complexed and their bioavailability to a single species in a mixed community is difficult to constrain. Further, Fe and P geochemistries are linked through the activities of metalloenzymes, such as the alkaline phosphatases (APs) PhoX and PhoA, which are used by microbes to access dissolved organic P (DOP). Here we identified significant correlations between Trichodesmium-specific transcriptional patterns in the North Atlantic (NASG) and North Pacific Subtropical Gyres (NPSG) and patterns in Fe and P biogeochemistry, with the relative enrichment of Fe stress markers in the NPSG, and P stress markers in the NASG. We also observed the differential enrichment of Fe-requiring PhoX transcripts in the NASG and Fe-insensitive PhoA transcripts in the NPSG, suggesting that metalloenzyme switching may be used to mitigate Fe limitation of DOP metabolism in Trichodesmium. This trait may underpin Trichodesmium success across disparate ecosystems.

Co-occurrence of Fe and P stress in natural populations of the marine diazotroph <i>Trichodesmium</i>

“…Because it can access a theoretically unlimited supply of atmospheric N 2 , Trichodesmium often becomes phosphorus (P) limited (Frischkorn et al, 2018;Hynes et al, 2009;Orchard, 2010;Sañudo-Wilhelmy et al, 2001;Wu et al, 2000). It also has a tendency to experience iron (Fe) limitation because the nitrogenase enzyme is iron-demanding (Bergman et al, 2013;Chappell et al, 2012;Rouco et al, 2018;Sunda, 2012;Walworth et al, 2016a).…”

<i>Trichodesmium</i> physiological ecology and phosphate reduction in the western tropical South Pacific

“…Geochemical drivers of Trichodesmium distribution and N 2 fixation are increasingly well characterized in regions of the ocean where either phosphorus or iron are limiting factors, such as the North Atlantic and North Pacific Subtropical Gyre (Rouco et al, 2018;Sañudo-Wilhelmy et al, 2001;Sohm et al, 2011). The western tropical South Pacific (WTSP) represents an understudied region of the world's oceans with conditions characterized by chronically low concentrations of both iron and phosphate (Moore et al, 2013;Sohm et al, 2011).…”

The Trichodesmium microbiome can modulate host N2 fixation

“…With the high‐iron quotas associated with N 2 fixation and photosynthesis, iron limitation is the canonical constraint on diazotrophy in Trichodesmium (Berman‐Frank et al ). In the oligotrophic western North Atlantic however, high‐iron concentrations relative to phosphorus lead to phosphorus depletion, and Trichodesmium distribution and N 2 fixation is thought to be more strongly influenced by phosphorus availability, relative to other systems (Sañudo‐Wilhelmy et al ; Moore et al ; Rouco et al , ). Despite the fact that resource controls on Trichodesmium eco‐physiology are well established, using geochemistry to predict and model the distribution and activities of this organism remains challenging (Capone et al ; McGillicuddy ; Snow et al ).…”