Decomposition rate and biochemical fate of carbon from natural polymers and microplastics in boreal lakes

Abstract

Microbial mineralization of organic compounds is essential for carbon recycling in food webs. Microbes can decompose terrestrial recalcitrant and semi-recalcitrant polymers such as lignin and cellulose, which are precursors for humus formation. In addition to naturally occurring recalcitrant substrates, microplastics have been found in various aquatic environments. However, microbial utilization of lignin, hemicellulose, and microplastics as carbon sources in freshwaters and their biochemical fate and mineralization rate in freshwaters is poorly understood. To fill this knowledge gap, we investigated the biochemical fate and mineralization rates of several natural and synthetic polymer-derived carbon in clear and humic lake waters. We used stable isotope analysis to unravel the decomposition processes of different 13C-labeled substrates [polyethylene, polypropylene, polystyrene, lignin/hemicellulose, and leaves (Fagus sylvatica)]. We also used compound-specific isotope analysis and molecular biology to identify microbes associated with used substrates. Leaves and hemicellulose were rapidly decomposed compared to microplastics which were degraded slowly or below detection level. Furthermore, aromatic polystyrene was decomposed faster than aliphatic polyethylene and polypropylene. The major biochemical fate of decomposed substrate carbon was in microbial biomass. Bacteria were the main decomposers of all studied substrates, whereas fungal contribution was poor. Bacteria from the family Burkholderiaceae were identified as potential leaf and polystyrene decomposers, whereas polypropylene and polyethylene were not decomposed.

Recycled by leaf inhabitants: Terrestrial bacteria drive the mineralization of organic matter in lake water

“…Our results suggest that OM quality does not affect the biochemical fate of carbon, but it has effects on the decomposition rate, as shown previously (e.g., Krevš et al, 2017;Muto et al, 2011). Among all leaf species, 80%-88% of leaf carbon taken up was respired daily, whereas the remaining 12%-20% of utilized leaf carbon was assimilated into biomass, supporting previous studies (Attermeyer et al, 2013;Taipale et al, 2023;Vesamäki et al, 2022). The assimilated carbon can be linked to aquatic food webs via grazers feeding on microbes, microbes thus being important connectors of terrestrial and aquatic ecosystems via carbon cycling (Attermeyer et al, 2013;Taipale et al, 2023).…”

“…During OM decomposition and microbial succession, the abundance and biomass of both fungi and bacteria change (Kuehn et al, 2000;Newman et al, 2015;Wardle, 1993). Although bacteria are generally considered to be more efficient in competing due to their better substrate utilization, faster population growth, and biomass production (Mille-Lindblom & Tranvik, 2003;Vesamäki et al, 2022), there has been debate about whether they actually participate in the decomposition or only assimilate leachates and byproducts of fungal decomposition (Purahong et al, 2016). Most studies suggest that fungi drive the leaf decomposition on leaves, whereas bacteria favor DOM and fine particulate organic carbon (e.g., Hayer et al, 2022;Kuehn, 2016;Zhao et al, 2017Zhao et al, , 2021.…”

The second life of terrestrial and plastic carbon as nutritionally valuable food for aquatic consumers

“…Numbers references OTU number (Table S1). Stress for 2 D MDS was 0.1. biodegradation of more recalcitrant lignin (van Erven et al, 2019;Vesamäki et al, 2022). Our results showed that easily degradable organic compounds are mainly used for energy, whereas more recalcitrant materials are preferably used as a carbon backbone for the synthesis of new biomolecules.…”

“…Conversely, we have recently revealed trophic uptake and conversion of plastic carbon to essential omega-3 (ω-3) and omega-6 (ω-6) polyunsaturated fatty acids (PUFA) (Taipale et al, 2019). This demonstrated trophic upgrading of microplastic (MP) carbon was an important finding since the persistence of MP in marine and freshwater ecosystems is an increasing environmental concern due to the predicted growth of slowly degrading plastic waste (Borrelle et al, 2020;Taipale et al, 2022;Vesamäki et al, 2022). Despite the slow process, direct utilization of some plastic blends and their leachates can support microbial biomass, complementing the trophic transfer of biomolecules (Sheridan et al, 2022;Taipale et al, 2019Taipale et al, , 2022Vesamäki et al, 2022;Yoshida et al, 2016).…”

“…However, microbial decomposition of recalcitrant organic carbon is generally slow and related to certain taxa including Actinobacteria and Proteobacteria (Bugg et al, 2011;Taipale et al, 2022;Vesamäki et al, 2022). These two phyla differ in their resistance to flagellate and zooplankton grazing, and thus, the microbial community structure can influence the trophic transfer of organic carbon (Taipale et al, 2012;Tarao et al, 2009).…”