Advancing Marker-Gene-Based Methods for Prokaryote-Mediated Multifunctional Redundancy: Exploring Random and Non-Random Extinctions in a Catchment

IF 2.8 2区生物学 Q2 ECOLOGY

Freshwater Biology Pub Date : 2025-03-16 DOI:10.1111/fwb.70020

Wan-Hsuan Cheng, Takeshi Miki, Motohiro Ido, Kinuyo Yoneya, Kazuaki Matsui, Taichi Yokokawa, Hiroki Yamanaka, Shin-ichi Nakano

{"title":"Advancing Marker-Gene-Based Methods for Prokaryote-Mediated Multifunctional Redundancy: Exploring Random and Non-Random Extinctions in a Catchment","authors":"Wan-Hsuan Cheng, Takeshi Miki, Motohiro Ido, Kinuyo Yoneya, Kazuaki Matsui, Taichi Yokokawa, Hiroki Yamanaka, Shin-ichi Nakano","doi":"10.1111/fwb.70020","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>\n \n </p><ol>\n \n \n <li>Multifunctional redundancy, which measures the extent of loss in multiple ecosystem functions with decreasing biodiversity, stands as a crucial index for evaluating ecosystem resilience to environmental changes. Previous studies have assessed functional redundancy by evaluating the overlap in multiple traits or functions among taxonomic units, but quantifying these experimentally for each taxonomic unit is challenging and resource-intensive, especially for microorganisms. In this study, we aimed to refine the estimation of multifunctional redundancy in prokaryotic communities using a marker-gene-based methodology.</li>\n \n \n <li>We used the bioinformatic tool, PICRUSt2, to predict KEGG ortholog (KO) composition for each Amplicon Sequence Variant (ASV) of the 16S rRNA gene and assessed community-wide KO richness as a metric of genomic multifunctionality. Additionally, we introduced a refined regression on KO richness vs. ASV richness curves, providing a reliable estimate of the power-law exponent within computational time constraints, serving as the multifunctional redundancy index. To quantify variations between different species extinction scenarios, we incorporated various non-random extinction scenarios alongside a random one. Finally, to elucidate potential mechanisms contributing to the variations in multifunctional redundancy, we applied our refined methodology to the prokaryote community in Lake Biwa and four of its inlet rivers.</li>\n \n \n <li>Our refined marker-gene-based methodology for quantifying multifunctional redundancy was effectively validated using experimentally quantified phenotypic multifunctionality. Our application to the Lake Biwa catchment revealed spatio-temporal variations in multifunctional redundancy.</li>\n \n \n <li>Our analysis demonstrated lower redundancy in Lake Biwa compared to its inlet rivers, aiding in prioritising conservation targets and inferring distinct community assembly processes.</li>\n \n \n <li>Future directions include a deeper exploration of KO composition information for detailed multifunctionality quantification and the refinement of extinction scenarios. This study demonstrates the promising integration of bioinformatic functional prediction and modelling biodiversity loss, offering a valuable tool for effective ecosystem management.</li>\n </ol>\n \n </div>","PeriodicalId":12365,"journal":{"name":"Freshwater Biology","volume":"70 3","pages":""},"PeriodicalIF":2.8000,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Freshwater Biology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/fwb.70020","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ECOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Multifunctional redundancy, which measures the extent of loss in multiple ecosystem functions with decreasing biodiversity, stands as a crucial index for evaluating ecosystem resilience to environmental changes. Previous studies have assessed functional redundancy by evaluating the overlap in multiple traits or functions among taxonomic units, but quantifying these experimentally for each taxonomic unit is challenging and resource-intensive, especially for microorganisms. In this study, we aimed to refine the estimation of multifunctional redundancy in prokaryotic communities using a marker-gene-based methodology.
We used the bioinformatic tool, PICRUSt2, to predict KEGG ortholog (KO) composition for each Amplicon Sequence Variant (ASV) of the 16S rRNA gene and assessed community-wide KO richness as a metric of genomic multifunctionality. Additionally, we introduced a refined regression on KO richness vs. ASV richness curves, providing a reliable estimate of the power-law exponent within computational time constraints, serving as the multifunctional redundancy index. To quantify variations between different species extinction scenarios, we incorporated various non-random extinction scenarios alongside a random one. Finally, to elucidate potential mechanisms contributing to the variations in multifunctional redundancy, we applied our refined methodology to the prokaryote community in Lake Biwa and four of its inlet rivers.
Our refined marker-gene-based methodology for quantifying multifunctional redundancy was effectively validated using experimentally quantified phenotypic multifunctionality. Our application to the Lake Biwa catchment revealed spatio-temporal variations in multifunctional redundancy.
Our analysis demonstrated lower redundancy in Lake Biwa compared to its inlet rivers, aiding in prioritising conservation targets and inferring distinct community assembly processes.
Future directions include a deeper exploration of KO composition information for detailed multifunctionality quantification and the refinement of extinction scenarios. This study demonstrates the promising integration of bioinformatic functional prediction and modelling biodiversity loss, offering a valuable tool for effective ecosystem management.

查看原文本刊更多论文

求助全文

约1分钟内获得全文求助全文

来源期刊

Freshwater Biology 生物-海洋与淡水生物学

CiteScore

5.90

自引率

3.70%

发文量

162

审稿时长

2 months

期刊介绍： Freshwater Biology publishes papers on all aspects of the ecology of inland waters, including rivers and lakes, ground waters, flood plains and other freshwater wetlands. We include studies of micro-organisms, algae, macrophytes, invertebrates, fish and other vertebrates, as well as those concerning whole systems and related physical and chemical aspects of the environment, provided that they have clear biological relevance. Studies may focus at any level in the ecological hierarchy from physiological ecology and animal behaviour, through population dynamics and evolutionary genetics, to community interactions, biogeography and ecosystem functioning. They may also be at any scale: from microhabitat to landscape, and continental to global. Preference is given to research, whether meta-analytical, experimental, theoretical or descriptive, highlighting causal (ecological) mechanisms from which clearly stated hypotheses are derived. Manuscripts with an experimental or conceptual flavour are particularly welcome, as are those or which integrate laboratory and field work, and studies from less well researched areas of the world. Priority is given to submissions that are likely to interest a wide range of readers. We encourage submission of papers well grounded in ecological theory that deal with issues related to the conservation and management of inland waters. Papers interpreting fundamental research in a way that makes clear its applied, strategic or socio-economic relevance are also welcome. Review articles (FRESHWATER BIOLOGY REVIEWS) and discussion papers (OPINION) are also invited: these enable authors to publish high-quality material outside the constraints of standard research papers.