Biodegradable dissolved organic carbon shapes bacterial community structures and co-occurrence patterns in large eutrophic Lake Taihu
Graphical abstract
Introduction
Interactions between dissolved organic matter (DOM) and bacteria play a key role in the biogeochemical cycles of aquatic ecosystems (Mou et al., 2008; Osterholz et al., 2015). DOM consists of various compounds and represents a large fraction of the global carbon pool (Coble, 2007). Bacterial degradation of DOM contributes to bacterial secondary production, nutrient recycling, and greenhouse outgassing, affecting the material circulation and energy flow in water bodies (Bertilsson et al., 2007; Guillemette et al., 2016). DOM quantity and quality are crucial factors shaping bacterial communities (Hur et al., 2011; Muscarella et al., 2019; Ruiz-González et al., 2015). Linkages between bacterial community and DOM composition have been evidenced for numerous systems (Kaartokallio et al., 2015; Logue et al., 2016). For instance, relationships between major bacterial clades and DOM fluorescence components have been established (Amaral et al., 2016; Melo et al., 2020), showing the importance of considering DOM characteristics when studying the interactions between DOM and bacteria.
The effect of DOM on bacterial communities is largely determined by its biodegradability depending on its chemical composition and molecular size (Berggren et al., 2010; Kellerman et al., 2015). Labile proteins and aliphatic compounds are rapidly utilized by bacteria (Guillemette et al., 2016), while the recalcitrant materials can be degraded only by specific groups (Landa et al., 2014). DOM with different biodegradability can cause distinct responses of bacterial diversity, community structure, and metabolism, as reflected in the carbon consumption, growth and respiration rate, as well as enzymatic degradation (Bana et al., 2014; Perez and Sommaruga, 2006; Roiha et al., 2016). Biodegradable dissolved organic carbon (BDOC) refers to the fraction of dissolved organic carbon (DOC) which can be removed by bacteria over a period of bioassay incubations (Hitchcock and Mitrovic, 2015). BDOC is a crucial parameter when examining the biogeochemical role of DOM in regards to global carbon fluxes (Vonk et al., 2015) and is an important component of the microbial loop (Nelson et al., 2011). Although the influence of BDOC on the bacterial community has been evidenced by incubating bacteria with different sources of DOM in lab studies (Guillemette et al., 2013; Perez and Sommaruga, 2006), the relative importance of BDOC compared with other environmental variables in structuring the bacterial communities in natural ecosystems needs further investigation.
Bacterial communities normally consist of a small number of abundant taxa and many rare species, as well as some “occasionally rare and abundant” taxa (Campbell et al., 2011). Taxa with distinct abundance patterns contribute differently to ecosystem function in terms of biomass, biodiversity, carbon flow, and nutrient cycling (Pedros-Alio, 2012). Moreover, different responses of these subcommunities to environmental changes have been evidenced, for example along elevation gradients (Li et al., 2017), changing in climatic regimes (Liang et al., 2020), algal blooms (Xue et al., 2018; Zhang et al., 2019a), and specific DOM amendment (Li et al., 2019). Moreover, bacteria interact with each other rather than live in isolation, thereby contributing to the overall composition, stability, and biodiversity of microbial ecosystems (Ratzke et al., 2020). Thus, it is important to consider species with different abundance patterns and their interactions when studying the linkages between bacterial communities and DOM. Thanks to high-throughput sequencing techniques and network analyses, rare subcommunities and complex cooccurrence networks between species can now be explored.
We investigated bacterial communities using 16S rRNA gene sequencing and chromophoric DOM (CDOM) characteristics as well as other physico-chemical variables and examined BDOC via bioassay incubations in a large eutrophic lake (Lake Taihu, China). Our objectives were to (i) examine the importance of BDOC for diversity, composition, and co-occurrence patterns of bacterial communities; (ii) compare the responses of abundant and rare bacterial communities with changes in key environmental variables including CDOM and BDOC characteristics. We hypothesized that BDOC is shaping bacterial community composition and co-occurrence patterns, being of particularly importance for the rare community, because rare taxa can include metabolically active species that can become dominant under favorable conditions by acting as bacterial “seed banks” (Lynch and Neufeld, 2015).
Section snippets
Study sites and sample collection
Lake Taihu is a large eutrophic lake located in the most developed region of eastern China with an area of 2338.1 km2. A total of 68 water samples were collected for CDOM optical measurements, including 32 samples collected from the whole lake in August 2018 and 36 samples collected monthly from three sites near the Taihu Laboratory for Lake Ecosystem Research (TLLER) from September 2018 to August 2019 (3 × 12) (Appendix A Fig. S1). Forty-seven of the 68 water samples were sequenced for
PARAFAC components and BDOC
The PARAFAC model-derived six components (Appendix A Fig. S2) were identified by comparison to the OpenFluor database (Murphy et al., 2014). The component C1 (Ex/Em = <230/436 nm) resembles humic-like DOM; C2 (250(340)/476 nm) represents terrestrial humic-like fluorophores (Shutova et al., 2014) and is associated with soil-derived fulvic acids (Osburn et al., 2016); C3 ((250)310/388 nm) represents microbial humic-like fluorophores (Osburn et al., 2016); C4 (<230(285)/340 nm) includes
Discussion
Our study revealed strong associations between the proportion of BDOC (%BDOC) and bacterial diversities, module structures of the co-occurrence network, and habitat niche breadths, as well as the relative abundance of key species. Moreover, the effect of environmental variables on bacterial community was most pronounced for the “conditionally rare and abundant” taxa subcommunities.
Our results support the concept that the biodegradability of DOC was highly related to CDOM quantity and chemical
Conclusions
Our results showed that the proportion of BDOC was significantly correlated with the concentration of DOC, BIX, the relative abundance of the tryptophan-like component, and CDOM aromaticity, indicating a strong linkage between autochthonous protein-like CDOM and BDOC in Lake Taihu. BDOC played a significant role in affecting bacterial community diversities, structures, and co-occurrence patterns and was more important than the majority of physico-chemical parameters including DOC. Increasing
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Nos. 41930760, 41807362, and 41977322), the Provincial Natural Science Foundation of Jiangsu in China (No. BK20181104), the Key Research Program of Frontier Sciences, Chinese Academy of Sciences (No. QYZDB-SSW-DQC016). Erik Jeppesen was supported by WATEC (Centre for Water Technology, AU) and the TÜBITAK outstanding scientists program 2232 (project 118C250). We would like to express our deep thanks to Anne Mette
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