Thermal Adaptation of Bacterial and Fungal Growth in a Geothermally Influenced Soil Transect

Numerous studies have investigated microbial adaptation to increasing soil temperature, but limitations in experimental design hinder comprehensive understanding. These include short-term laboratory studies with constant environmental conditions and field studies with few distinct temperature treatments. Here, we utilized a long-term natural soil geothermal gradient in Aotearoa, New Zealand, ranging in mean annual soil temperature (MAT) from 17°C to 42°C to explore thermal adaptation of microbial growth rates. We collected soil from 28 locations along the gradient and measured bacterial growth rate (via leucine incorporation) at eight temperatures (4°C-45°C) and fungal growth rate (via Ac-in-ergosterol) at two temperatures (16°C and 39°C). We then fit Macromolecular Rate Theory and the Ratkowsky equation to estimate the temperature minimum ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>min</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{min} $$</mml:annotation></mml:semantics> </mml:math> ), optimum ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>opt</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{opt} $$</mml:annotation></mml:semantics> </mml:math> ), and inflection point ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>inf</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{inf} $$</mml:annotation></mml:semantics> </mml:math> ) for bacterial growth, and a temperature sensitivity index to compare relative fungal and bacterial growth rates. We found predictable changes in thermal adaptation of bacterial growth along the geothermal gradient with temperature response curves shifting 0.22°C-0.27°C per 1°C increase in MAT regardless of the temperature metric (i.e., <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>min</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{min} $$</mml:annotation></mml:semantics> </mml:math> , <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>opt</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{opt} $$</mml:annotation></mml:semantics> </mml:math> , and <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics> <mml:mrow><mml:msub><mml:mi>T</mml:mi> <mml:mi>inf</mml:mi></mml:msub> </mml:mrow> <mml:annotation>$$ {T}_{inf} $$</mml:annotation></mml:semantics> </mml:math> ) used. Thermal adaptation of bacterial and fungal growth increased roughly in parallel. We also compared the bacterial growth results to published temperature response data of microbial respiration (with added glucose) from this geothermal gradient. Rates of thermal adaptation for bacterial growth and microbial respiration were similar, suggesting synchronicity across microbial processes. The less than 1°C change in all measured temperatures metrics per degree increase in MAT resulted in microbial growth and activity closer to in situ temperatures at high soil temperatures and lower than in situ temperatures under non-elevated soil temperatures. Overall, our results highlight the use of geothermal gradients and appropriate temperature models in studying thermal adaptation of soil microbial processes; the predictability of results also underscores potential for incorporating microbial thermal adaptation into soil carbon modeling efforts.