Freshwater lake ecosystem is a reservior of valuable microbial diversity. It needs to be explored for addressing key environmental issues like petroleum-hydrocarbon contamination. In this work, the microbial communities (pre and post enriched with petroleum-hydrocarbons) from different layers of freshwater lake, i.e. surface water, sediments and deepwater, were explored through metagenomic and culture-dependent approaches. A total of 41 bacterial phyla were retrieved from pre-enriched samples, which were significantly reduced in enriched samples where Proteobacteria were dominant (87% to 100%) followed by Bacteroidetes (7.37%) and Verrucomicrobia (3.06%). The most dominant hydrocarbon-degrading genera were extensively verified as Pseudomonas (48.65%), Acinetobacter (45.38%), Stenotrophomonas (3.16%) and Brevundimonas (2.07%) in surface water (S1WCC); Acinetobacter (62.46%), Aeromonas (10.7%), Sphingobacterium (5.20%) and Pseudomonas (4.23%) in sediment (S2MCC); and Acinetobacter (46.57%), Pseudomonas (13.10%), Comamonas (12.93%), Flavobacterium (12.18%) and Enterobacter (9.62%) in deep water (S4WCC). Additionally, the maximum biodegradation of petroleum-hydrocarbons (i.e. used engine oil or UEO) was achieved by microbiome of S2MCC (67.60 ± 0.08%) followed by S4WCC (59.70 ± 0.12%), whereas only 36.80 ± 0.10% degradation was achieved by S1WCC microbiome. On the other hand, UEO degradation by cultivable biosurfactant-producing single cultures such as Pseudomonas sp. S2WE, Pseudomonas sp. S2WG, Pseudomonas sp. S2MS, Ochrobactrum sp. S1MM and Bacillus nealsonii S2MT showed 31.10 ± 0.08% to 40.50 ± 0.11% biodegradation. Comparatively, the biodegradation efficiency was found higher (i.e. 42.20 ± 0.12% to 56.10 ± 0.12%) in each consortia comprising of two, three, four, and five bacterial cultures. Conclusively, the isolated culturable biosurfactants-producing bacterial consortium of freshwater lake demonstrated >80% contribution in the total petroleum-hydrocarbons degradation by the natural microbiome of the ecosystem.